Skip to main content
SpringerLink
Log in

Identification and characterization of two xyloglucan-specific endo-1,4-glucanases in Aspergillus oryzae

  • Biotechnologically relevant enzymes and proteins
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Aspergillus oryzae produces glycoside hydrolases to degrade xyloglucan. We identified and characterized two xyloglucan-specific endo-1,4-glucanases (xyloglucanases) named Xeg12A and Xeg5A. Based on their amino acid sequences, Xeg12A and Xeg5A were classified into glycoside hydrolase families GH12 and GH5, respectively. Xeg12A degrades tamarind seed xyloglucan polysaccharide into xyloglucan oligosaccharides containing four glucopyranosyl residues as main chains, including heptasaccharides (XXXG: Glc4Xyl3), octasaccharides (XXLG and XLXG: Glc4Xyl3Gal1), and nonasaccharides (XLLG: Glc4Xyl3Gal2). By contrast, Xeg5A produces various xyloglucan oligosaccharides from xyloglucan. Xeg5A hydrolyzes xyloglucan into not only XXXG, XXLG/XLXG, and XLLG but also disaccharides (isoprimeverose: Glc1Xyl1), tetrasaccharides (XX: Glc2Xyl2 and LG: Glc2Xyl1Gal1), and so on. Xeg12A is a typical endo-dissociative-type xyloglucanase that repeats hydrolysis and desorption from xyloglucan. Conversely, Xeg5A acts as an endo-processive-type xyloglucanase that hydrolyzes xyloglucan progressively without desorption. These results indicate that although both Xeg12A and Xeg5A contribute to the degradation of xyloglucan, they have different modes of activity toward xyloglucan, and the hydrolysis machinery of Xeg5A is unique compared with that of other known GH5 enzymes.

Key points

• We identified two xyloglucanases, Xeg12A and Xeg5A, in A. oryzae.

• Modes of activity and regiospecificities of Xeg12A and Xeg5A were clearly different.

• Xeg5A is a unique xyloglucanase that produces low-molecular-weight oligosaccharides.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Agger JW, Isaksen T, Várnai A, Vidal-Melgosa S, Willats WG, Ludwig R, Horn SJ, Eijsink VG, Westereng B (2014) Discovery of LPMO activity on hemicelluloses shows the importance of oxidative processes in plant cell wall degradation. Proc Natl Acad Sci U S A 111:6287–6292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arnal G, Stogios PJ, Asohan J, Attia MA, Skarina T, Viborg AH, Henrissat B, Savchenko A, Brumer H (2019) Substrate specificity, regiospecificity, and processivity in glycoside hydrolase family 74. J Biol Chem 294:13233–13247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arnal G, Stogios PJ, Asohan J, Skarina T, Savchenko A, Brumer H (2018) Structural enzymology reveals the molecular basis of substrate regiospecificity and processivity of an exemplar bacterial glycoside hydrolase family 74 endo-xyloglucanase. Biochem J 475:3963–3978

    Article  CAS  PubMed  Google Scholar 

  • Aspeborg H, Coutinho PM, Wang Y, Brumer H III, Henrissat B (2012) Evolution, substrate specificity and subfamily classification of glycoside hydrolase family 5 (GH5). BMC Evol Biol 12:186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Attia MA, Brumer H (2016) Recent structural insights into the enzymology of the ubiquitous plant cell wall glycan xyloglucan. Curr Opin Structural Biol 40:43–53

    Article  CAS  Google Scholar 

  • Augur C, Yu L, Sasaki K, Ogawa T, Sinay P, Darvill AL, Albersheim P (1992) Further studies of the ability of xyloglucan oligosaccharides to inhibit auxin-stimulated growth. Plant Physiol 99:180–185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bauer S, Vasu P, Mort AJ, Somerville CR (2005) Cloning, expression, and characterization of an oligoxyloglucan reducing end-specific xyloglucanobiohydrolase from Aspergillus nidulans. Carbohydr Res 340:2590–2597

    Article  CAS  PubMed  Google Scholar 

  • Bauer S, Vasu P, Persson S, Mort AJ, Somerville CR (2006) Development and application of a suite of polysaccharide-degrading enzymes for analyzing plant cell walls. Proc Natl Acad Sci U S A 103:11417–11422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bennati-Granier C, Garajova S, Champion C, Grisel S, Haon M, Zhou S, Fanuel M, Ropartz D, Rogniaux H, Gimbert I, Record E, Berrin JG (2015) Substrate specificity and regioselectivity of fungal AA9 lytic polysaccharide monooxygenases secreted by Podospora anserina. Biotechnol Biofuels 8:90

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Carpita NC, Gibeaut DM (1993) Structure models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3:1–30

    Article  CAS  PubMed  Google Scholar 

  • Chaillou S, Lokman BC, Leer RJ, Posthuma C, Postma PW, Pouwels PH (1998) Cloning, sequence analysis, and characterization of the genes involved in isoprimeverose metabolism in Lactobacillus pentosus. J Bacteriol 180:2312–2320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Damasio AR, Rubio MV, Gonçalves TA, Persinoti GF, Segato F, Prade RA, Contesini FJ, de Souza AP, Buckeridge MS, Squina FM (2017) Xyloglucan breakdown by endo-xyloglucanase family 74 from Aspergillus fumigatus. Appl Microbiol Biotechnol 101:2893–2903

    Article  CAS  PubMed  Google Scholar 

  • Edwards M, Dea IC, Bulpin PV, Reid JS (1986) Purification and properties of a novel xyloglucan-specific endo-(1→4)-β-d-glucanase from germinated nasturtium seeds (Tropaeolum majus L.). J Biol Chem 261:9489–9494

    Article  CAS  PubMed  Google Scholar 

  • Fox JD, Robyt JF (1991) Miniaturization of three carbohydrate analyses using a microsample plate reader. Anal Biochem 195:93–96

    Article  CAS  PubMed  Google Scholar 

  • Fry SC, York WS, Albersheim P, Darvill A, Hayashi T, Joseleau J-P, Kato Y, Lorences EP, Maclachlan GA, McNeil M, Mort AJ, Grant Reid JS, Seitz HU, Selvendran RR, Voragen AGJ, White AR (1993) An unambiguous nomenclature for xyloglucan-derived oligosaccharides. Physiol Plant 89:1–3

    Article  CAS  Google Scholar 

  • Gloster TM, Ibatullin FM, Macauley K, Eklöf JM, Roberts S, Turkenburg JP, Bjørnvad ME, Jørgensen PL, Danielsen S, Johansen KS, Borchert TV, Wilson KS, Brumer H, Davies GJ (2007) Characterization and three-dimensional structures of two distinct bacterial xyloglucanases from families GH5 and GH12. J Biol Chem 282:19177–19189

    Article  CAS  PubMed  Google Scholar 

  • Grishutin SG, Gusakov AV, Markov AV, Ustinov BB, Semenova MV, Sinitsyn AP (2004) Specific xyloglucanases as a new class of polysaccharide-degrading enzymes. Biochim Biophys Acta 1674:268–281

    Article  CAS  PubMed  Google Scholar 

  • Hamamoto T, Foong F, Shoseyov O, Doi RH (1992) Analysis of functional domains of endoglucanases from Clostridium cellulovorans by gene cloning, nucleotide sequencing and chimeric protein construction. Mol Gen Genet 231:472–479

    Article  CAS  PubMed  Google Scholar 

  • Hashimoto T, Nakata Y (2003) Synergistic degradation of arabinoxylan with α-l-arabinofuranosidase, xylanase and β-xylosidase from soy sauce koji mold, Aspergillus oryzae, in high salt condition. J Biosci Bioeng 95:164–169

    Article  CAS  PubMed  Google Scholar 

  • Hasper AA, Dekkers E, van Mil M, van de Vondervoort PJ, de Graaff LH (2002) EglC, a new endoglucanase from Aspergillus niger with major activity towards xyloglucan. Appl Environ Microbiol 68:1556–1560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He H, Qin Y, Li N, Chen G, Liang Z (2015) Purification and characterization of a thermostable hypothetical xylanase from Aspergillus oryzae HML366. Appl Microbiol Biotechnol 175:3148–3161

    CAS  Google Scholar 

  • Hemsworth GR, Thompson AJ, Stepper J, Sobala ŁF, Coyle T, Larsbrink J, Spadiut O, Goddard-Borger ED, Stubbs KA, Brumer H, Davies GJ (2016) Structural dissection of a complex Bacteroides ovatus gene locus conferring xyloglucan metabolism in the human gut. Open Biol 6:160142

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Henrissat B, Teeri TT, Warren RA (1998) A scheme for designating enzymes that hydrolyse the polysaccharides in the cell walls of plants. FEBS Lett 425:352–354

    Article  CAS  PubMed  Google Scholar 

  • Jagadeeswaran G, Gainey L, Prade R, Mort AJ (2016) A family of AA9 lytic polysaccharide monooxygenases in Aspergillus nidulans is differentially regulated by multiple substrates and at least one is active on cellulose and xyloglucan. Appl Microbiol Biotechnol 100:4535–4547

    Article  CAS  PubMed  Google Scholar 

  • Jørgensen PL, Hansen CK (1990) Multiple endo-beta-1,4-glucanase-encoding genes from Bacillus lautus PL236 and characterization of the celB gene. Gene 93:55–60

    Article  PubMed  Google Scholar 

  • Kato Y, Matsushita J, Kubodera T, Matsuda K (1985) A novel enzyme producing isoprimeverose from oligoxyloglucans of Aspergillus oryzae. J Biochem 97:801–810

    Article  CAS  PubMed  Google Scholar 

  • Kimura T, Suzuki H, Furuhashi H, Aburatani T, Morimoto K, Karita S, Sakka K, Ohmiya K (2000) Molecular cloning, overexpression, and purification of a major xylanase from Aspergillus oryzae. Biosci Biotechnol Biochem 64:2734–2738

    Article  CAS  PubMed  Google Scholar 

  • Kimura T, Suzuki H, Furuhashi H, Aburatani T, Morimoto K, Sakka K, Ohmiya K (2002) Molecular cloning, characterization, and expression analysis of the xynF3 gene from Aspergillus oryzae. Biosci Biotechnol Biochem 66:285–292

    Article  CAS  PubMed  Google Scholar 

  • Kitamoto N, Go M, Shibayama T, Kimura T, Kito Y, Ohmiya K, Tsukagoshi N (1996) Molecular cloning, purification and characterization of two endo-1,4-β-glucanases from Aspergillus oryzae KBN616. Appl Microbiol Biotechnol 46:538–544

    Article  CAS  PubMed  Google Scholar 

  • Kitamoto N, Yoshino S, Ito M, Kimura T, Ohmiya K, Tsukagoshi N (1998) Repression of the expression of genes encoding xylanolytic enzymes in Aspergillus oryzae by introduction of multiple copies of the xynF1 promoter. Appl Microbiol Biotechnol 50:558–563

    Article  CAS  PubMed  Google Scholar 

  • Kitamoto N, Yoshino S, Ohmiya K, Tsukagoshi N (1999a) Sequence analysis, overexpression, and antisense inhibition of a β-xylosidase gene, xylA, from Aspergillus oryzae KBN616. Appl Environ Microbiol 65:20–24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kitamoto N, Yoshino S, Ohmiya K, Tsukagoshi N (1999b) Purification and characterization of the overexpressed Aspergillus oryzae xylanase, XynF1. Biosci Biotechnol Biochem 63:1791–1794

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi T, Abe K, Asai K, Gomi K, Juvvadi PR, Kato M, Kitamoto K, Takeuchi M, Machida M (2007) Genomics of Aspergillus oryzae. Biosci Biotechnol Biochem 71:646–670

    Article  CAS  PubMed  Google Scholar 

  • Kojima K, Várnai A, Ishida T, Sunagawa N, Petrovic DM, Igarashi K, Jellison J, Goodell B, Alfredsen G, Westereng B, Eijsink VG, Yoshida M (2016) A lytic polysaccharide monooxygenase with broad xyloglucan specificity from the brown-rot fungus Gloeophyllum trabeum and its action on cellulose-xyloglucan complexes. Appl Environ Microbiol 82:6557–6572

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larsbrink J, Izumi A, Ibatullin FM, Nakhai A, Gilbert HJ, Davies GJ, Brumer H (2011) Structural and enzymatic characterization of a glycoside hydrolase family 31 α-xylosidase from Cellvibrio japonicus involved in xyloglucan saccharification. Biochem J 436:567–580

    Article  CAS  PubMed  Google Scholar 

  • Larsbrink J, Rogers TE, Hemsworth GR, McKee LS, Tauzin AS, Spadiut O, Klinter S, Pudlo NA, Urs K, Koropatkin NM, Creagh AL, Haynes CA, Kelly AG, Cederholm SN, Davies GJ, Martens EC, Brumer H (2014a) A discrete genetic locus confers xyloglucan metabolism in select human gut Bacteroides. Nature 506:498–502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larsbrink J, Thompson AJ, Lundqvist M, Gardner JG, Davies GJ, Brumer H (2014b) A complex gene locus enables xyloglucan utilization in the model saprophyte Cellvibrio japonicus. Mol Microbiol 94:418–433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42:D490–D495

    Article  CAS  PubMed  Google Scholar 

  • Machida M, Asai K, Sano M, Tanaka T, Kumagai T, Terai G, Kusumoto K, Arima T, Akita O, Kashiwagi Y, Abe K, Gomi K, Horiuchi H, Kitamoto K, Kobayashi T, Takeuchi M, Denning DW, Galagan JE, Nierman WC, Yu J, Archer DB, Bennett JW, Bhatnagar D, Cleveland TE, Fedorova ND, Gotoh O, Horikawa H, Hosoyama A, Ichinomiya M, Igarashi R, Iwashita K, Juvvadi PR, Kato M, Kato Y, Kin T, Kokubun A, Maeda H, Maeyama N, Maruyama J, Nagasaki H, Nakajima T, Oda K, Okada K, Paulsen I, Sakamoto K, Sawano T, Takahashi M, Takase K, Terabayashi Y, Wortman JR, Yamada O, Yamagata Y, Anazawa H, Hata Y, Koide Y, Komori T, Koyama Y, Minetoki T, Suharnan S, Tanaka A, Isono K, Kuhara S, Ogasawara N, Kikuchi H (2005) Genome sequencing and analysis of Aspergillus oryzae. Nature 438:1157–1161

    Article  PubMed  Google Scholar 

  • Martinez-Fleites C, Guerreiro CI, Baumann MJ, Taylor EJ, Prates JA, Ferreira LM, Fontes CM, Brumer H, Davies GJ (2006) Crystal structures of Clostridium thermocellum xyloglucanase, XGH74A reveal the structural basis for xyloglucan recognition and degradation. J Biol Chem 281:24922–24933

    Article  CAS  PubMed  Google Scholar 

  • Master ER, Zheng Y, Storms R, Tsang A, Powlowski J (2008) A xyloglucan-specific family 12 glycosyl hydrolase from Aspergillus niger: recombinant expression, purification and characterization. Biochem J 411:161–170

    Article  CAS  PubMed  Google Scholar 

  • Matsuzawa T, Kameyama A, Yaoi K (2018) A novel isoprimeverose-producing enzyme from Phaeoacremonium minimum is active with low concentrations of xyloglucan oligosaccharides. FEBS Open Bio 9:92–100

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Matsuzawa T, Kameyama A, Yaoi K (2020) Identification and characterization of α-xylosidase involved in xyloglucan degradation in Aspergillus oryzae. Appl Microbiol Biotechnol 104:201–210

    Article  CAS  PubMed  Google Scholar 

  • Matsuzawa T, Kimura N, Suenaga H, Yaoi K (2016a) Screening, identification, and characterization of α-xylosidase from a soil metagenome. J Biosci Bioeng 122:393–399

    Article  CAS  PubMed  Google Scholar 

  • Matsuzawa T, Mitsuishi Y, Kameyama A, Yaoi K (2016b) Identification of the gene encoding isoprimeverose-producing oligoxyloglucan hydrolase in Aspergillus oryzae. J Biol Chem 291:5080–5087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsuzawa T, Saito Y, Yaoi K (2014) Key amino acid residues for the endo-processive activity of GH74 xyloglucanase. FEBS Lett 588:1731–1738

    Article  CAS  PubMed  Google Scholar 

  • Matsuzawa T, Watanabe M, Kameda T, Kameyama A, Yaoi K (2019a) Cooperation between β-galactosidase and an isoprimeverose-producing oligoxyloglucan hydrolase is key for xyloglucan degradation in Aspergillus oryzae. FEBS J 286:3182–3193

    Article  CAS  PubMed  Google Scholar 

  • Matsuzawa T, Watanabe M, Nakamichi Y, Fujimoto Z, Yaoi K (2019b) Crystal structure and substrate recognition mechanism of Aspergillus oryzae isoprimeverose-producing enzyme. J Struct Biol 205:84–90

    Article  CAS  PubMed  Google Scholar 

  • Matsuzawa T, Yaoi K (2016) GH74 xyloglucanases: structures and modes of activity. Trends Glycosci Glycotechnol 28:E63–E70

  • McDougall GJ, Fry SC (1989) Structure-activity relationship for xyloglucan oligosaccharides with antiauxin activity. Plant Physiol 89:883–887

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McGregor N, Morar M, Fenger TH, Stogios P, Lenfant N, Yin V, Xu X, Evdokimova E, Cui H, Henrissat B, Savchenko A, Brumer H (2016) Structure-function analysis of a mixed-linkage β-glucanase/xyloglucanase from the key ruminal Bacteroidetes Prevotella bryantii B14. J Biol Chem 291:1175–1197

  • McIlvaine TC (1921) A buffer solution for colorimetric comparison. J Biol Chem 49:183–186

    Article  CAS  Google Scholar 

  • Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428

    Article  CAS  Google Scholar 

  • Minetoki T, Gomi K, Kitamoto K, Kumagai C, Tamura G (1995) Nucleotide sequence and expression of α-glucosidase-encoding gene (agdA) from Aspergillus oryzae. Biosci Biotechnol Biochem 59:1516–1521

    Article  CAS  PubMed  Google Scholar 

  • Moracci M, Cobucci Ponzano B, Trincone A, Fusco S, De Rose M, van Der Oost J, Sensen CW, Charlebois RL, Rossi M (2000) Identification and molecular characterization of the first α-xylosidase from an Archaeon. J Biol Chem 275:22082–22089

    Article  CAS  PubMed  Google Scholar 

  • Nguyen CH, Tsurumizu R, Sato T, Takeuchi M (2005) Taka-amylase A in the conidia of Aspergillus oryzae RIB40. Biosci Biotechnol Biochem 69:2035–2041

    Article  CAS  PubMed  Google Scholar 

  • Okuyama M, Mori H, Chiba S, Kimura A (2004) Overexpression and characterization of two unknown proteins, YicI and YihQ, originated from Escherichia coli. Protein Expr Purif 37:170–179

    Article  CAS  PubMed  Google Scholar 

  • Pauly M, Andersen LN, Kauppinen S, Kofod LV, York WS, Albersheim P, Darvill A (1999) A xyloglucan-specific endo-β-1,4-glucanase from Aspergillus aculeatus: expression cloning in yeast, purification and characterization of the recombinant enzyme. Glycobiology 9:93–100

    Article  CAS  PubMed  Google Scholar 

  • Powlowski J, Mahajan S, Schapira M, Master ER (2009) Substrate recognition and hydrolysis by a fungal xyloglucan-specific family 12 hydrolase. Carbohydr Res 344:1175–1179

    Article  CAS  PubMed  Google Scholar 

  • Sakai K, Mochizuki M, Yamada M, Shinzawa Y, Minezawa M, Kimoto S, Murata S, Kaneko Y, Ishihara S, Jindou S, Kobayashi T, Kato M, Shimizu M (2017) Biochemical characterization of thermostable β-1,4-mannase belonging to the glycoside hydrolase family 134 from Aspergillus oryzae. Appl Microbiol Biotechnol 101:3237–3245

    Article  CAS  PubMed  Google Scholar 

  • Sato Y, Fukuda H, Zhou Y, Mikami S (2010) Contribution of ethanol-tolerant xylosidase G2 from Aspergillus oryzae on Japanese sale brewing. J Biosci Bioeng 110:679–683

    Article  CAS  PubMed  Google Scholar 

  • Scott-Craig JS, Borrusch MS, Banerjee G, Harvey CM, Walton JD (2011) Biochemical and molecular characterization of secreted α-xylosidase from Aspergillus niger. J Biol Chem 286:42848–42854

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki S, Fukuoka M, Ookuchi H, Sano M, Ozeki K, Nagayoshi E, Takii Y, Matsushita M, Tada S, Kusumoto K, Kashiwagi Y (2010) Characterization of Aspergillus oryzae hydrolase family 43 β-xylosidase expressed in Escherichia coli. J Biosci Bioeng 109:115–117

    Article  CAS  PubMed  Google Scholar 

  • Tsukagoshi N, Furukawa M, Nagaba H, Kirita N, Tsuboi A, Udaka S (1989) Isolation of a cDNA encoding Aspergillus oryzae Taka-amylase A: evidence for multiple related genes. Gene 84:319–327

  • Tuomivaara ST, Yaoi K, O’Neill MA, York WS (2015) Generation and structural validation of a library of diverse xyloglucan-derived oligosaccharides, including an update on xyloglucan nomenclature. Carbohydr Res 402:56–66

    Article  CAS  PubMed  Google Scholar 

  • Wirsel S, Lachmund A, Wildhardt G, Ruttkowski E (1989) Three α-amylase genes of Aspergillus oryzae exhibit identical intron-exon organization. Mol Microbiol 3:3–14

    Article  CAS  PubMed  Google Scholar 

  • Wu M, McNulty NP, Rodionov DA, Khoroshkin MS, Griffin NW, Cheng J, Latreille P, Kerstetter RA, Terrapon N, Henrissat B, Osterman AL, Gordon J (2015) Genetic determinants of in vivo fitness and diet responsiveness in multiple human gut Bacteroides. Science 350:aac5992

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yaoi K, Mitsuishi Y (2002) Purification, characterization, cloning, and expression of a novel xyloglucan-specific glycosidase, oligoxyloglucan reducing end-specific cellobiohydrolase. J Biol Chem 277:48276–48281

  • Yaoi K, Mitsuishi Y (2004) Purification, characterization, cDNA cloning, and expression of a xyloglucan endoglucanase from Geotrichum sp. M128. FEBS Lett 560:45–50

  • Yaoi K, Nakai T, Kameda Y, Hiyoshi A, Mitsuishi Y (2005) Cloning and characterization of two xyloglucanases from Paenibacillus sp. strain KM21. Appl Environ Microbiol 71:7670–7678

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • York WS, Darvill AG, Albersheim P (1984) Inhibition of 2,4-dichlorophenoxyacetic acid-stimulated elongation of pea stem segments by a xyloglucan oligosaccharide. Plant Physiol 75:295–297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshikawa K, Yamamoto K, Okada S (1994) Classification of some α-glucosidases and α-xylosidases on the basis of substrate specificity. Biosci Biotechnol Biochem 58:1392–1398

    Article  CAS  PubMed  Google Scholar 

  • Zabotina OA (2012) Xyloglucan and its biosynthesis. Front Plant Sci 3:134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We thank the National Research Institute of Brewing (Hiroshima, Japan) for the A. oryzae RIB40 strain.

Funding

This study was supported by the Japan Society for the Promotion of Science KAKENHI (Grant-in-Aid for Scientific Research B, grant no. 18H02132).

Author information

Authors and Affiliations

  1. Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), 1-1-1 Higashi, Tsukuba, Ibaraki, 305-8566, Japan

    Tomohiko Matsuzawa & Katsuro Yaoi

  2. Biotechnology Research Institute for Drug Discovery, National Institute of Advanced Industrial Science and Technology (AIST), 1-1-1 Higashi, Tsukuba, Ibaraki, 305-8565, Japan

    Akihiko Kameyama

  3. Research Institute for Sustainable Chemistry, National Institute of Advanced Industrial Science and Technology (AIST), 3-11-32, Kagamiyama, HigashiHiroshima, Hiroshima, 739-0046, Japan

    Yusuke Nakamichi

Authors
  1. Tomohiko Matsuzawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Akihiko Kameyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yusuke Nakamichi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Katsuro Yaoi
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

TM conceived and designed the experiments. AK analyzed the oligosaccharides. YN purified xyloglucanases. TM performed and analyzed all other experiments. TM, AK, YN and KY wrote the paper.

Corresponding author

Correspondence to Tomohiko Matsuzawa.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(PDF 3542 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Matsuzawa, T., Kameyama, A., Nakamichi, Y. et al. Identification and characterization of two xyloglucan-specific endo-1,4-glucanases in Aspergillus oryzae. Appl Microbiol Biotechnol 104, 8761–8773 (2020). https://doi.org/10.1007/s00253-020-10883-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-020-10883-7

Keywords

Search

Navigation