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Review

Plant-Polysaccharide-Degrading Enzymes from Basidiomycetes

Johanna Rytioja, Kristiina Hildén, Jennifer Yuzon, Annele Hatakka, Ronald P. de Vries, Miia R. Mäkelä
Johanna Rytioja
aDepartment of Food and Environmental Sciences, Division of Microbiology and Biotechnology, University of Helsinki, Helsinki, Finland
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Kristiina Hildén
aDepartment of Food and Environmental Sciences, Division of Microbiology and Biotechnology, University of Helsinki, Helsinki, Finland
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Jennifer Yuzon
bFungal Physiology, CBS-KNAW Fungal Biodiversity Centre, Utrecht, The Netherlands
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Annele Hatakka
aDepartment of Food and Environmental Sciences, Division of Microbiology and Biotechnology, University of Helsinki, Helsinki, Finland
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Ronald P. de Vries
bFungal Physiology, CBS-KNAW Fungal Biodiversity Centre, Utrecht, The Netherlands
cFungal Molecular Physiology, Utrecht University, Utrecht, The Netherlands
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Miia R. Mäkelä
aDepartment of Food and Environmental Sciences, Division of Microbiology and Biotechnology, University of Helsinki, Helsinki, Finland
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DOI: 10.1128/MMBR.00035-14
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    FIG 1

    Simplified model of plant cell wall structure. (A) The structure consists of three main layers: the middle lamella and the primary and secondary walls. (A and B) The main polysaccharides and lignin which form the surrounding structure for the plasma membrane are presented in the primary (B) and secondary wall (C). The lignin content in the primary cell wall (not illustrated) varies considerably depending on the plant species (Table 1). The illustrations are not to scale.

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    FIG 2

    Schematic representation of plant cell wall polysaccharides and selected corresponding polysaccharide-degrading enzymes. (A) Cellulose; (B) xyloglucan; (C) β-glucan; (D) heteroxylan; (E) heteromannan; (F) pectin. Enzyme abbreviations are presented in Table 2. Polysaccharide structures were drawn by using data reported previously by Mohnen (203) and Doblin et al. (204).

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    FIG 3

    Average molecular masses (kDa for monomers) (A), isoelectric points (pI) (B), pH optima (C), and temperature optima (D) of selected CAZymes from basidiomycetous (first columns, in dark colors) and Aspergillus species (second columns, in light colors). EG, endoglucanase; CBH, cellobiohydrolase; BGL, β-glucosidase; XLN, endoxylanase; MAN, endomannanase; MND, β-mannosidase; AGL, α-galactosidase; AGU, α-glucuronidase; CDH, cellobiose dehydrogenase. The number of characterized enzymes used for calculation of mean values is marked at the root of each column. Error bars show the minimum and maximum values reported for each biochemical characteristic. −, no mean value was available.

Tables

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  • TABLE 1

    Approximate chemical compositions of softwood, hardwood, monocot, and dicot plant cell wallsa

    Plant materialChemical composition (% dry wt)b
    CelluloseHemicellulosesPectinLignin
    MannanXylanβ-GlucanXyloglucan
    Softwood33–4210–155–11———27–32
    Hardwood38–472–515–30———21–31
    Monocots
        Primary20–30Minor20–4010–301–55Minor
        Secondary35–45Minor40–50MinorMinorMinor20
    Dicots
        Primary15–305–105ND20–2520–30Minor
        Secondary45–503–520–30NDMinorMinor7–10
    • ↵a Data were obtained from references 20 and 22.

    • ↵b —, not reported; ND, not detected.

  • TABLE 2

    Plant-polysaccharide-degrading enzymes

    SubstrateEnzyme activityEC no.aAbbreviationCAZyme family(ies)
    Celluloseβ-1,4-Endoglucanase3.2.1.4EGGH3, -5, -6, -7, -9, -12, -45
    Cellobiohydrolase (reducing end)3.2.1.176CBHIGH7
    Cellobiohydrolase (nonreducing end)3.2.1.91CBHIIGH6
    β-1,4-Glucosidase3.2.1.21BGLGH1, -3
    Cellobiose dehydrogenase1.1.99.18CDHAA3_1, AA8
    Lytic polysaccharide monooxygenaseNALPMOAA9
    Xylanβ-1,4-Endoxylanase3.2.1.8XLNGH10, -11
    Xylobiohydrolase3.2.1.–XBH
    β-1,4-Xylosidase3.2.1.37BXLGH3, -43
    Galactomannanβ-1,4-Endomannanase3.2.1.78MANGH5, -26
    β-1,4-Mannosidase3.2.1.25MNDGH2
    β-1,4-Galactosidase3.2.1.23LACGH2, -35
    α-1,4-Galactosidase3.2.1.22AGLGH27, -36
    α-Arabinofuranosidase3.2.1.55ABFGH51, -54
    Galactomannan acetyl esterase3.1.1.–GMAE
    XyloglucanXyloglucan β-1,4-endoglucanase3.2.1.151XEGGH12, -74
    α-Arabinofuranosidase3.2.1.55ABFGH51, -54
    α-Xylosidase3.2.1.177AXLGH31
    α-Fucosidase3.2.1.51AFCGH29, -95
    α-1,4-Galactosidase3.2.1.22AGLGH27, -36
    β-1,4-Galactosidase3.2.1.23LACGH2, -35
    ArabinoxylanArabinoxylan arabinofuranohydrolase/arabinofuranosidase3.2.1.55AXHGH62
    α-Glucuronidase3.2.1.139AGUGH67, -115
    α-1,4-Galactosidase3.2.1.22AGLGH27, -36
    β-1,4-Galactosidase3.2.1.23LACGH2, -35
    Acetyl xylan esterase3.1.1.72AXECE1, -5
    Feruloyl esterase3.1.1.73FAECE1
    PectinEndopolygalacturonases3.2.1.15PGAGH28
    Exopolygalacturonases3.2.1.67PGXGH28
    Xylogalacturonan hydrolase3.2.1.–XGH
    Endorhamnogalacturonase3.2.1.171RHGGH28
    Exorhamnogalacturonase3.2.1.–RHXGH28
    Rhamnogalacturonan rhamnohydrolase3.2.1.174RGXBGH28
    α-Rhamnosidase3.2.1.40RHAGH78
    α-Arabinofuranosidase3.2.1.55ABFGH51, -54, -62
    Endoarabinanase3.2.1.99ABNGH43
    Exoarabinanase3.2.1.–ABXGH93
    β-1,4-Endogalactanase3.2.1.89GALGH53
    Unsaturated glucuronyl hydrolase3.2.1.–UGHGH88
    Unsaturated rhamnogalacturonan hydrolase3.2.1.172URHGH105
    β-1,4-Xylosidase3.2.1.37BXLGH3, -43
    β-1,4-Galactosidase3.2.1.23LACGH2, -35
    Pectin lyase4.2.2.10PELPL1
    Pectate lyase4.2.2.2PLYPL1, -3, -9
    Rhamnogalacturonan lyase4.2.2.23RGLPL4, -11
    Pectin methyl esterase3.1.1.11PMECE8
    Pectin acetyl esterase3.1.1.–PAE
    Rhamnogalacturonan acetyl esterase3.1.1.–RGAECE12
    Feruloyl esterase3.1.1.73FAECE1
    • ↵a NA, not categorized by the International Union of Biochemistry and Molecular Biology (IUBMB).

  • TABLE 3

    List of basidiomycete species with published genomes and CAZyme annotations

    EcologySpeciesWebsite(s)Reference(s)
    White rotAuricularia subglabrahttp://genome.jgi.doe.gov/Aurde3_1/Aurde3_1.home.html11
    Bjerkandera adustahttp://genome.jgi.doe.gov/Bjead1_1/Bjead1_1.home.html205
    Ceriporiopsis (Gelatoporia) subvermisporahttp://genome.jgi.doe.gov/Cersu1/Cersu1.home.html12
    Dichomitus squalenshttp://genome.jgi-psf.org/Dicsq1/Dicsq1.home.html11
    Fomitiporia mediterraneahttp://genome.jgi-psf.org/Fomme1/Fomme1.home.html11
    Ganoderma lucidumhttp://www.herbalgenomics.org/galu/14
    Ganoderma sp.http://genome.jgi.doe.gov/Gansp1/Gansp1.home.html205
    Heterobasidion irregularehttp://genome.jgi-psf.org/Hetan2/Hetan2.home.html66
    Phanerochaete carnosahttp://genome.jgi.doe.gov/Phaca1/Phaca1.home.html45
    Phanerochaete chrysosporiumhttp://genome.jgi-psf.org/Phchr2/Phchr2.home.html6, 57
    Phlebia brevisporahttp://genome.jgi.doe.gov/Phlbr1/Phlbr1.home.html205
    Pleurotus ostreatushttp://genome.jgi.doe.gov/PleosPC15_2/PleosPC15_2.home.html55
    Punctularia strigosozonatahttp://genome.jgi-psf.org/Punst1/Punst1.home.html11
    Stereum hirsutumhttp://genome.jgi-psf.org/Stehi1/Stehi1.home.html11
    Trametes versicolorhttp://genome.jgi-psf.org/Trave1/Trave1.home.html11
    White rot-likeSchizophyllum communehttp://genome.jgi-psf.org/Schco3/Schco3.home.html15
    Uncertain classificationBotryobasidium botryosumhttp://genome.jgi.doe.gov/Botbo1/Botbo1.home.html55
    Jaapia argillaceahttp://genome.jgi.doe.gov/Jaaar1/Jaaar1.home.html55
    Brown rotConiophora puteanahttp://genome.jgi-psf.org/Conpu1/Conpu1.home.html11
    Dacryopinax sp.http://genome.jgi-psf.org/Dacsp1/Dacsp1.home.html11
    Fomitopsis pinicolahttp://genome.jgi-psf.org/Fompi3/Fompi3.home.html11
    Gloeophyllum trabeumhttp://genome.jgi-psf.org/Glotr1_1/Glotr1_1.home.html11
    Postia placentahttp://genome.jgi-psf.org/Pospl1/Pospl1.home.html18
    Serpula lacrymans S7.3http://genome.jgi-psf.org/SerlaS7_3_2/SerlaS7_3_2.home.html71
    Serpula lacrymans S7.9http://genome.jgi-psf.org/SerlaS7_9_2/SerlaS7_9_2.home.html71
    Wolfiporia cocoshttp://genome.jgi-psf.org/Wolco1/Wolco1.home.html11
    Litter decomposingAgaricus bisporus var. bisporushttp://genome.jgi-psf.org/Agabi_varbisH97_2/Agabi_varbisH97_2.home.html9
    Agaricus bisporus var. burnettiihttp://genome.jgi.doe.gov/Agabi_varbur_1/Agabi_varbur_1.home.html9
    Galerina marginatahttp://genome.jgi.doe.gov/Galma1/Galma1.home.html55
    Straw decomposingVolvariella volvaceahttp://www.ncbi.nlm.nih.gov/genome/?term=Volvariella+volvacea13
    CoprophilicCoprinopsis cinereahttp://genome.jgi-psf.org/Copci1/Copci1.home.html206
    Plant pathogenicMelampsora laricis-populinahttp://genome.jgi.doe.gov/Mellp1/Mellp1.home.html10
    Puccinia graminishttp://genome.jgi-psf.org/Pucgr1/Pucgr1.home.html10
    Ustilago maydishttp://www.broad.mit.edu/annotation/genome/ustilago_maydis/Home.html, http://mips.gsf.de/genre/proj/ustilago/8
    ParasiticTremella mesentericahttp://genome.jgi-psf.org/Treme1/Treme1.home.html11
    EctomycorrhizaLaccaria bicolorhttp://genome.jgi-psf.org/Lacbi2/Lacbi2.home.html, http://mycor.nancy.inra.fr/IMGC/LaccariaGenome/7
    Piriformospora indicahttp://genome.jgi-psf.org/Pirin1/Pirin1.home.html77
    YeastCryptococcus neoformans var. grubiihttp://genome.jgi.doe.gov/Cryne_H99_1/Cryne_H99_1.home.html81
    Rhodotorula glutinishttp://www.ncbi.nlm.nih.gov/nuccore/AEVR0000000082
    Mold-likeWallemia sebihttp://genome.jgi.doe.gov/Walse1/Walse1.home.html207
  • TABLE 4

    Distribution of CAZyme-encoding genes in basidiomycetes and Aspergillus speciesd

    TABLE 4
    • a No β-N-acetylhexosaminidase was included.

    • b β-1,4-Endoglucanase and β-1,4-endomannanase are included.

    • c Can also include models associated with more than one category.

    • ↵d Gene numbers are based on previously reported data for the following organisms, and basidiomycete data are updated according to Riley et al. (55): Agaricus bisporus var. bisporus (9), Aspergillus fumigatus (208), Aspergillus nidulans (49, 209), Aspergillus niger (ATCC 1015) (84, 210), Aspergillus oryzae (211), Auricularia subglabra (11), Bjerkandera adusta (205), Botryobasidium botryosum (55), Ceriporiopsis subvermispora (12), Coniophora puteana (11), Coprinopsis cinerea (206), Cryptococcus neoformans var. grubii (81), Dacryopinax sp. (11), Dichomitus squalens (11), Fomitiporia mediterranea (11), Fomitopsis pinicola (11), Galerina marginata (55), Ganoderma lucidum (14), Ganoderma sp. (205), Gloeophyllum trabeum (11), Heterobasidion irregulare (66), Jaapia argillacea (55), Laccaria bicolor (7), Melampsora laricis-populina (10), Phanerochaete carnosa (45), Phanerochaete chrysosporium (6), Phlebia brevispora (205), Piriformospora indica (77), Pleurotus ostreatus (55), Postia placenta (18), Puccinia graminis (10), Punctularia strigosozonata (11), Rhodotorula glutinis (82), Schizophyllum commune (15), Serpula lacrymans 7.9 (71), Stereum hirsutum (11), Trametes versicolor (11), Tremella mesenterica (11), Ustilago maydis (8), Wallemia sebi (207), Wolfiporia cocos (11), and Volvariella volvacea (13). †, white rot-like; *, ecological classification uncertain; —, not in published papers.

  • TABLE 5

    Characterized basidiomycete β-1,4-endoglucanases and their biochemical properties

    Life-styleSpeciesCAZyme familyGeneEnzymeaNCBI protein database accession no.bMolecular mass (kDa)pIpHoptTopt (°C)Reference(s)
    White rotCerrena unicolor444.0212
    Dichomitus squalensEn I424.84.855213
    D. squalensEn II564.34.855213
    D. squalensEn III474.14.855213
    Ganoderma lucidum554.716
    G. lucidum434.716
    Irpex lacteus564.050214
    I. lacteusEn-1164.050215
    I. lacteusE2-A216
    I. lacteusE2-B216
    I. lacteusGH5En-1*38217
    Phanerochaete chrysosporiumGH5cel5AEG36AAU12275365.6–5.758, 90
    P. chrysosporiumGH5cel5AEG38AAU12275384.958, 90
    P. chrysosporiumGH5cel5BEG44444.358, 90
    P. chrysosporiumGH12cel12ACel12AAAU12276285.258, 91
    P. chrysosporiumGH45PcCel45A1892
    Polyporus arculariusCMCase I394.4–4.668218
    P. arculariusCMCase II364.4–4.668218
    P. arculariusGH3cel3ACMCase IIIaBAD98315244.952218, 219
    Sporotrichum pulverulentumcT1325.3220
    S. pulverulentumcT2a374.7220
    S. pulverulentumcT2b284.4220
    S. pulverulentumcT3a384.7220
    S. pulverulentumcT3b374.2220
    Trametes hirsutaGH5ThEG44221
    T. hirsutaGH5rEG*505.050221
    Trametes versicolor30222, 223
    Brown rotConiophora cerebellaA424.7224
    C. cerebellaB394.2224
    Fomitopsis palustris40225
    F. palustrisGH5EG4747105
    F. palustrisEG3535105
    F. palustrisGH12cel12106
    F. palustrisGH12eg2EGIIBAF49602243.555226
    Gloeophyllum sepiarium (Lenzites sepiaria)85227
    G. sepiariumEGS453.84.159108
    Gloeophyllum trabeumEGT413.14.262108
    G. trabeumGH5Cel5A424.9103
    G. trabeumGH12Cel12A28103
    G. trabeum (Lenzites trabea)294.470145
    Serpula incrassataCel 2525<3.650228
    S. incrassataCel 4949<3.6228
    S. incrassataCel 5757<3.6228
    Piptoporus betulinusEG1622.6–2.83.570109
    Postia placenta35–40229
    Straw decomposingVolvariella volvaceaGH5eg1EG1AAG59832427.77.55589, 230
    Plant pathogenPolyporus schweinitzii454.060231, 232
    Sclerotium rolfsiiEndo A524.64.074233
    S. rolfsiiEndo B274.22.3–3.050233
    S. rolfsiiEndo C784.54.050233
    Ustilago maydisGH45egl1Egl1AAB3614793
    YeastRhodotorula glutinis408.64.550234
    • ↵a Asterisks indicate a heterologously produced enzyme.

    • ↵b See http://www.ncbi.nlm.nih.gov/protein.

    • ↵c Anamorph of P. chrysosporium.

  • TABLE 6

    Characterized basidiomycete cellobiohydrolases and their biochemical properties

    Life-styleSpeciesCAZyme familyGeneEnzymeNCBI protein database accession no.aMolecular mass (kDa)pIpHoptTopt (°C)Reference(s)
    White rotDichomitus squalensEx 1394.65.060235
    D. squalensEx 2364.55.060235
    D. squalensGH7cel7bCDJ7966561
    Flammulina velutipesGH7cel7aFvCel7ABAJ0753450236
    F. velutipesGH7cel7bFvCel7BBAJ0753560236
    Ganoderma lucidum565.216
    G. lucidum495.016
    G. lucidum505.616
    Irpex lacteusGH7cel1Ex-1BAA76363534.55.050189, 237
    I. lacteusGH7cel2Ex-2BAA76364564.85.050189
    I. lacteusGH7cel3BAA76365238
    I. lacteusGH6cex3BAG481836050239
    I. lacteus655.050240
    Lentinula edodesGH7cel7ACEL7AAAK95563241
    L. edodesGH6cel6BCEL6BAAK95564241
    Phanerochaete chrysosporiumGH7cbh1-1Cel7ACAA3827495, 192, 242
    P. chrysosporiumGH7cbh1-2Cel7BCAA3827595, 192, 242
    P. chrysosporiumGH7cbh1Cel7CAAB46373624.994, 95, 192, 242, 243
    P. chrysosporiumGH7cbh1-4Cel7DAAA19802583.894, 95, 244
    P. chrysosporiumGH7cbh1-5Cel7E95
    P. chrysosporiumGH7cbh1-6/7Cel7F/G6, 95, 242
    P. chrysosporiumGH6CBH50504.994
    P. chrysosporiumGH6cbhIICBHIIAAB32942245
    Polyporus arculariusGH7cel1BAF80326246
    P. arculariusGH6cel2BAF80327246
    Brown rotConiophora puteanaCBHI523.65.0107
    C. puteanaCBHII503.65.0107
    Fomitopsis palustris4.570104
    Litter decomposingAgaricus arvensisGH7HM004552b130c4.065247
    Agaricus bisporusGH6cel3ACCEL3AAA5060752186
    A. bisporusGH7cel2CAA90422133
    Straw decomposingVolvariella volvaceaGH7cbhICBHIAAD4109698
    V. volvaceaGH6cbhIICBHIIAAD4109798
    CoprophilicCoprinopsis cinereaGH6CcCel6ACcCel6ABAH08702248, 249
    C. cinereaGH6CcCel6BCcCel6BBAH08703248, 249
    C. cinereaGH6CcCel6CCcCel6CBAH08704248, 249
    C. cinereaGH6CcCel6DBAH08705249
    C. cinereaGH6CcCel6EBAH08706249
    White rot plant pathogenHeterobasidion irregulareGH7HirCel7A504.04597
    Plant pathogenSclerotium rolfsii41.5–42.04.34.237250
    Insect symbiontTermitomyces sp.GH6Cellulase IF524.4251
    • ↵a See http://www.ncbi.nlm.nih.gov/protein.

    • ↵b Gene identifier.

    • ↵c Dimer.

  • TABLE 7

    Characterized basidiomycete β-glucosidases and their biochemical properties

    Life-styleSpeciesCAZyme familyGeneEnzymeaNCBI protein database accession no.bMolecular mass (kDa)pIpHoptTopt (°C)Reference(s)
    White rotCeriporiopsis (Gelatoporia) subvermispora1103.560252
    C. subvermispora533.560252
    Fomes fomentarius586.74.5–5.060100
    Phanerochaete chrysosporium905.545101
    P. chrysosporium4107.045101
    P. chrysosporium454.75.060253
    P. chrysosporium1144.0–5.2254
    P. chrysosporiumGH3cbgl-1AAC26490255
    P. chrysosporiumGH3cbgl-2AAC26489255
    P. chrysosporiumGH3wtBGLBAB85988116256, 257
    P. chrysosporiumGH3rBGL*BAB85988133257
    P. chrysosporiumGH1bgl1ABG1A*BAE8700853113
    P. chrysosporiumGH1bgl1BBG1B*BAE8700960113
    Pleurotus ostreatusF1357.54.04099
    P. ostreatusF2507.34.05099
    P. ostreatusF3668.55.05099
    Trametes gibbosa6403.540–50258
    Trametes versicolor3004.345185, 259
    Sporotrichum pulverulentumcA11654.84.0–4.5260
    S. pulverulentumcA21724.54.0–4.5260
    S. pulverulentumcB1-3165–1824.6–5.24.0–4.5260
    Stereum hirsutumBGL98261
    White rot-likeSchizophyllum commune975.3262
    S. communeI1023.45.8263
    S. communeII963.35.1263
    Brown rotFomitopsis palustrisGH3Cel3ACel3A*NR705.060146
    Gloeophyllum trabeum (Lenzites trabea)3204.575145, 264
    Piptoporus betulinusBG1362.64.060109
    Poria vaillantii4.250265
    Litter decomposingAgaricus bisporusbg1CAC03462—d
    Straw decomposingVolvariella volvaceaBGL-I1585.67.055–60102
    V. volvaceaBGL-II2565.0–5.26.255–60102
    V. volvaceaGH3bglAAG5983195266
    Plant pathogenSclerotium rolfsiiBG-1904.14.268187
    S. rolfsiiBG-2904.64.268187
    S. rolfsiiBG-31075.14.268187
    S. rolfsiiBG-4925.64.268187
    Ustilago esculentaGH3UeBgl3A*BAK618081105.040267
    EctomycorrhizaTricholoma matsutake1605.060268
    Pisolithus tinctorius450e3.84.065269
    Insect symbiontTermitomyces clypeatus1165.045270
    T. clypeatus1104.55.065271
    YeastRhodotorula minuta1444.84.7–5.270188
    Sporobolomyces singularisGH1bglABglABAD95570743.545112
    • ↵a Asterisks indicate a heterologously produced enzyme. wtBGL, wild-type BGL.

    • ↵b See http://www.ncbi.nlm.nih.gov/protein. NR, not reported.

    • ↵c Anamorph of P. chrysosporium.

    • ↵d Available in the GenBank database (http://www.ncbi.nlm.nih.gov/GenBank/).

    • ↵e Trimer.

  • TABLE 8

    Characterized basidiomycete cellobiose dehydrogenases and lytic polysaccharide monooxygenases, their biochemical properties, and their corresponding genes

    Life-styleSpeciesCAZyme family(ies)GeneEnzymeaNCBI protein database accession no.bMolecular mass (kDa)pIpHoptcToptc (°C)Reference(s)
    Cellobiose dehydrogenase
        White rotCeriporiopsis subvermisporaAA3_1, AA8cdhACF6061787–983.04.560116
    Irpex lacteusCDHII974.0d50d118
    Phanerochaete chrysosporiumcdhAAC49277894.25.0272, 273
    P. chrysosporiumcdhCDH*CAA61359904.23.5–4d274–276
    Pycnoporus cinnabarinuscdhAAC32197923.84.575277, 278
    P. cinnabarinusCDHI815.95.5279
    P. cinnabarinusCDHII1013.84.5279
    P. cinnabarinusCDH*ADX416881104.570280
    Trametes hirsuta924.25.0e60–70117
    Trametes pubescensTpCDH904.24.5–5.0e119
    Trametes versicolorAA3_1, AA8cdhCDH 4.2*AAC50004974.24.555281–283
    T. versicolorAA3_1CDH 6.46.455281
    Trametes villosaTvCDH894.44.5–5.0e119
    Grifola frondosacdhGfrCDHBAC20641284
    Phlebia lindtnericdhAGE456791044.05.0e60e285
    Pycnoporus sanguineusAA3_1, AA81134.24.570286
        White rot-likeSchizophyllum commune102287
        Brown rotConiophora puteana1113.9120, 121
        CoprophilicCoprinopsis cinereaAA3_1, AA8CDHcc*∼805.060114
        Plant pathogenSclerotium rolfsiiAA3_1, AA81014.2–5.03.2–4.855288, 289
    Lytic polysaccharide monooxygenases
        White rotHeterobasidion irregulareAA9HiGH61AGH61AAFO72232290
    H. irregulareAA9HiGH61BGH61BAFO72233290
    H. irregulareAA9HiGH61C290
    H. irregulareAA9HiGH61DGH61DAFO72234290
    H. irregulareAA9HiGH61E290
    H. irregulareAA9HiGH61FAFO72235290
    H. irregulareAA9HiGH61GAFO72236290
    H. irregulareAA9HiGH61HAFO72237290
    H. irregulareAA9HiGH61IAFO72238290
    H. irregulareAA9HiGH61JAFO72239290
    Phanerochaete chrysosporiumAA9PcGH61D*254.8125
    • ↵a Asterisks indicate a heterologously produced enzyme.

    • ↵b See http://www.ncbi.nlm.nih.gov/protein.

    • ↵c Activity measured with 2,6-dichlorophenolindophenol (DCIP) and cellobiose.

    • ↵d Activity measured with cytochrome c.

    • ↵e Activity measured with DCIP and lactose.

  • TABLE 9

    Characterized basidiomycete β-1,4-endoxylanases and β-xylosidases and their biochemical properties

    Life-styleSpeciesCAZyme familyGeneEnzymeaNCBI protein database accession no.bMolecular mass (kDa)pIpHoptTopt (°C)Reference
    Endoxylanase
        White rotCeriporiopsis (Gelatoporia) subvermisporaXylanase I798.050128
    C. subvermispora295.060291
    Cerrena unicolor444.0212
    Ganoderma lucidumXylanase B315.416
    Irpex lacteus387.6–8.04.6–5.260292
    I. lacteusXylanase I386.060293
    I. lacteusXylanase III626.070293
    Lentinula edodes413.64.5–5.060294
    L. edodesGH11xyn11AXYN11A*AAL041524.550295
    L. edodesGH10354.050296
    Phanerochaete chrysosporiumGH10xynAXynA*ABZ88797524.570297
    P. chrysosporiumGH11xynBXynB*ABZ88798304.560297
    P. chrysosporiumGH10xynCXynC*ABZ88799504.570297
    P. chrysosporiumGH10XynAXynA*AEK97220505.070298
    P. chrysosporiumGH10XynCXynC*AEK97221555.070299
    P. chrysosporiumGH10XynAXYNA*AAG4499248300
    P. chrysosporiumGH11XynBXYNB*AAG4499537300
    Phlebia radiataXA-1196.7131
    P. radiataXA-2164.1131
    Pycnoporus cinnabarinus504.05.060277
        White rot-likeSchizophyllum communeGH11Xylanase A335.055301
    S. communeGH10XynB312.85.550302
    S. communeXynC303.65.550302
        Brown rotGloeophyllum trabeum39–425.04.080303
    G. trabeumGH10Xyn10A394.8103
    G. trabeumGH10Xyn10A*AFR330463.450129
    G. trabeumGH10Xyn10B*AFR330474.570129
    G. trabeumGH10Xyl10gAEJ35165—c
    Laetiporus sulfureus693.080304
    Postia placenta433.8305
        Litter decomposingAgaricus bisporusGH10xynAXLNA*CAB0566534190
        CoprophilicCoprinopsis cinereaGH11Xyn11C*AFR330496.550–60129
        Insect symbiontTermitomyces clypeatus905.555306
    Termitomyces sp.875.665–70307
    β-Xylosidase
        White rotPhanerochaete chrysosporiumGH43PcXylrPcXyl*AFW16059835.045130
    Phlebia radiataXD-1275.9131
        Plant pathogenSclerotium rolfsii1704.550308
    • ↵a Asterisks indicate a heterologously produced enzyme.

    • ↵b See http://www.ncbi.nlm.nih.gov/protein.

    • ↵c Available in the GenBank database (http://www.ncbi.nlm.nih.gov/GenBank/).

  • TABLE 10

    Characterized basidiomycete β-1,4-endomannanases and mannosidases and their biochemical properties

    Life-styleSpeciesCAZyme familyGeneEnzymeaNCBI protein database accession no.bMolecular mass (kDa)pIpHoptTopt (°C)Reference(s)
    β-Endomannanase
        White rotCeriporiopsis (Gelatoporia) subvermisporaMannanase I1504.560128
    Heterobasidion irregulare (Fomes annosus)3.9–4.2309
    Phanerochaete chrysosporiumGH5man5DMan5D*ABG79370654.0–6.060132
    P. chrysosporiumGH5man5CABG79371—c
    P. chrysosporium (Chrysosporium lignorum)4.11309
        Litter decomposingAgaricus bisporusGH5Cel4b133, 134
        Plant pathogenSclerotium rolfsii613.52.974135, 136, 310, 311
    S. rolfsii423.23.372135, 310
    S. rolfsii472.83.0–3.575138
    Stereum sanguinolentum3.58309
    β-Mannosidase
        White rotGanoderma lucidum494.216
    G. lucidum494.816
    Phlebia radiataGM-11054.85.550141
    P. radiataGM-2903.85.550141
    P. radiataOT-11004.75.550141
        Brown rotLaetiporus (Polyporus) sulfureus642.4–3.4142
        Plant pathogenSclerotium rolfsii584.52.555135
    • ↵a Asterisks indicate a heterologously produced enzyme.

    • ↵b See (http://www.ncbi.nlm.nih.gov/protein).

    • ↵c Available in the GenBank database (http://www.ncbi.nlm.nih.gov/GenBank/).

  • TABLE 11

    Characterized basidiomycete pectin-degrading enzymes and their biochemical properties

    Life-styleSpeciesCAZyme familyGeneEnzymeaNCBI protein database accession no.bMolecular mass (kDa)pI(s)pHoptTopt (°C)Reference(s)
    Endo/exopolygalacturonases and rhamnogalacturonases
        White rotPhanerochaete chrysosporium424.3, 4.6, 4.74.766147
        Plant pathogenChondrostereum purpureumGH28epgAAAF68401150
    C. purpureumGH28epgB1AAF68402150
    C. purpureumGH28epgB2AAK29433150
    C. purpureumGH28epgCAAF68403150
    C. purpureumGH28epgDAAF68404150
    C. purpureumGH28cppg1PGABAA96351149
    C. purpureumGH28Pg1PGABAA08102398.8148
    Sclerotium (Corticium) rolfsiiPGA2.5151
    S. rolfsii46–485.24.0152
    S. rolfsii28–315.24.0152
        YeastCystofilobasidium capitatumPGA4445153, 154
    Rhamnogalacturonan hydrolase
        White rotIrpex lacteusRGH*ACI26689557.24.5–5.040–50155, 156
    • ↵a The asterisk indicates a heterologously produced enzyme.

    • ↵b See http://www.ncbi.nlm.nih.gov/protein.

  • TABLE 12

    Characterized basidiomycete-debranching enzymes and their biochemical properties

    Life-styleSpeciesCAZyme familyGeneEnzymeaNCBI protein database accession no.bMolecular mass (kDa)pIpHoptTopt (°C)Reference(s)
    α-Arabinofuranosidase
        White rotDichomitus squalens605.13.560312
        CoprophilicCoprinopsis cinereaGH62CcAbf62ACcAbf62A*BAK14423487.045313
    α-Galactosidase
        White rotGanoderma lucidum494.616
    G. lucidum249c6.070166
    Lenzites elegansGH36158d4.0–4.24.560–80167
    Phanerochaete chrysosporiumGH27AAG24510, AAG24511250c3.75165, 314
    Phlebia radiataAgaS-b1607.25.060169
    P. radiataAgaS-b2595.75.060169
    P. radiataAgaS-b3603.55.060169
    P. radiataAgaS-m1556.75.060169
    P. radiataAgaS-m2585.75.060169
    P. radiataAgaS-m3645.05.060169
    Pleurotus florida994.6–5.055168
        SaprobicCalvatia cyathiformis3.0–5.050315
    β-Galactosidase
        Plant pathogenSclerotium (Corticium) rolfsii2.0–2.5316
        YeastSporobolomyces (Bullera) singularis535.050317
    β-1,3-Endo/exogalactanase
        White rotFlammulina velutipesGH16FvEn3GALFvEn3GAL*BAK48741305.550318
    Irpex lacteusGH43Il1,3GalrIl1,3Gal*BAH29957454.540319
    Galactan β-1,3-galactosidase
        White rotPhanerochaete chrysosporiumGH431,3Gal43A1,3Gal43A*BAD9824155320
    α-Glucuronidase
        White rotPhanerochaete chrysosporium1124.63.5160
    Phlebia radiata1104.43.860161
        White rot-likeSchizophyllum communeGH115Agu1Agu1*ADV52250163
    S. commune1253.64.5–5.5162
        Litter decomposingAgaricus bisporus3.352321
    Acetyl xylan esterase
        White rotPhanerochaete chrysosporiumCE1axe158
    P. chrysosporiumCE1PcAxe2PcAxe2*AEX99751637.030–35170
        White rot-likeSchizophyllum commune317.730–45322
        Straw decomposingVolvariella volvaceaVvaxe1VvAXE1*ABI63599458.060323
        CoprophilicCoprinopsis cinereaeCcEst1CcEst1*BAJ1085745324
    Feruloyl esterase
        White rotAuricularia auricula-judaeEstBC363.26.561–66175
    Pleurotus eryngiiFaeA675.25.050173
    Pleurotus sapidusEst1556.050174
    Pectin methyl esterase
        Plant pathogenSclerotium (Corticium) rolfsii372.5–4.545159
    • ↵a Asterisks indicate a heterologously produced enzyme.

    • ↵b See http://www.ncbi.nlm.nih.gov/protein.

    • ↵c Tetramer.

    • ↵d Dimer.

    • ↵e Acetic acid- and ferulic acid-releasing activities.

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Plant-Polysaccharide-Degrading Enzymes from Basidiomycetes
Johanna Rytioja, Kristiina Hildén, Jennifer Yuzon, Annele Hatakka, Ronald P. de Vries, Miia R. Mäkelä
Microbiology and Molecular Biology Reviews Nov 2014, 78 (4) 614-649; DOI: 10.1128/MMBR.00035-14

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Plant-Polysaccharide-Degrading Enzymes from Basidiomycetes
Johanna Rytioja, Kristiina Hildén, Jennifer Yuzon, Annele Hatakka, Ronald P. de Vries, Miia R. Mäkelä
Microbiology and Molecular Biology Reviews Nov 2014, 78 (4) 614-649; DOI: 10.1128/MMBR.00035-14
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  • Top
  • Article
    • SUMMARY
    • INTRODUCTION
    • PLANT CELL WALL POLYSACCHARIDES
    • ENZYMES MODIFYING PLANT POLYSACCHARIDES
    • BASIDIOMYCETE GENOMES AND PLANT POLYSACCHARIDE DEGRADATION
    • CHARACTERIZED PLANT CELL WALL POLYSACCHARIDE-DEGRADING ENZYMES IN BASIDIOMYCETES AND Aspergillus
    • REGULATION OF PLANT POLYSACCHARIDE DEGRADATION IN BASIDIOMYCETES AND Aspergillus
    • CONCLUSIONS AND FUTURE PROSPECTS
    • ACKNOWLEDGMENTS
    • REFERENCES
    • Author Bios
  • Figures & Data
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