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Mycology

Comparative Transcriptome and Secretome Analysis of Wood Decay Fungi Postia placenta and Phanerochaete chrysosporium

Amber Vanden Wymelenberg, Jill Gaskell, Michael Mozuch, Grzegorz Sabat, John Ralph, Oleksandr Skyba, Shawn D. Mansfield, Robert A. Blanchette, Diego Martinez, Igor Grigoriev, Philip J. Kersten, Dan Cullen
Amber Vanden Wymelenberg
1Department of Bacteriology, University of Wisconsin, Madison, Wisconsin 53706
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Jill Gaskell
2USDA Forest Service, Forest Products Laboratory, Madison, Wisconsin 53726
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Michael Mozuch
2USDA Forest Service, Forest Products Laboratory, Madison, Wisconsin 53726
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Grzegorz Sabat
3Genetics and Biotechnology Center, University of Wisconsin, Madison, Wisconsin 53706
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John Ralph
4Department of Biochemistry and Department of Energy, Great Lakes Bioenergy Research Center, University of Wisconsin, Madison, Wisconsin 53726
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Oleksandr Skyba
5Department of Wood Science, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada
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Shawn D. Mansfield
5Department of Wood Science, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada
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Robert A. Blanchette
6Department of Plant Pathology, University of Minnesota, St. Paul, Minnesota 55108
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Diego Martinez
7Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131
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Igor Grigoriev
8Department of Energy, Joint Genome Institute, Walnut Creek, California 94598
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Philip J. Kersten
2USDA Forest Service, Forest Products Laboratory, Madison, Wisconsin 53726
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Dan Cullen
2USDA Forest Service, Forest Products Laboratory, Madison, Wisconsin 53726
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  • For correspondence: dcullen@facstaff.wisc.edu
DOI: 10.1128/AEM.00058-10
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  • FIG. 1.
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    FIG. 1.

    Heat map showing hierarchical clustering of Phanerochaete chrysosporium genes exhibiting highly significant (P < 0.001) accumulation of transcripts in aspen-grown versus glucose-grown cultures. Numbers within boxes indicate the fold difference in transcripts for aspen versus glucose cultures. Only those P. chrysosporium genes exceeding a 4-fold difference are shown. Underlined P. chrysosporium models correspond to genes with >50 cDNA tags in medium containing powdered oak (43). On the right, a heat map shows transcript levels of the most closely related P. placenta sequences or, in the absence of a clear homolog, labeled as “None.” Protein IDs followed by asterisks correspond to peptides unambiguously identified by LC-MS/MS in filtrates from aspen-grown cultures. The log2-based scales below maps are calibrated to the data shown above. Boldface denotes models in need of editing: GH10 xylanase model Ppl113670 has been superceded by an annotated preferred version, Ppl134783, which shows less pronounced upregulation (1.10) with a log2 signal of 11.3. GH27 α-galactosidase model Ppl128150 has been superceded by annotated preferred version Ppl13470, which shows more pronounced upregulation (3.08) with a log2 signal of 14.4 (Table 3; see also Table S1 in the supplemental material for detailed data).

  • FIG. 2.
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    FIG. 2.

    Heat map showing hierarchical clustering of P. placenta genes exhibiting highly significant (P < 0.001) accumulation of transcripts in aspen-grown versus glucose-grown cultures. Numbers within boxes indicate the fold difference in transcripts in aspen versus glucose cultures. Only those P. placenta genes exceeding a 4-fold difference are shown. On right is a heat map showing transcript levels of the most closely related P. chrysosporium sequences or, in the absence of a clear homolog, labeled as “None.” Protein IDs followed by asterisks correspond to peptides unambiguously identified by MS in filtrates from aspen-grown cultures. Scales below maps show log2-based signals. Underlined P. chrysosporium models correspond to genes with >50 cDNA tags in medium containing powdered oak (43).

  • FIG. 3.
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    FIG. 3.

    Transcript levels of P. placenta genes encoding copper radical oxidases (Ppl130305, Ppl56703, and Ppl64380), GMC oxidoreductases with distant similarity to glucose oxidase (GOX; Ppl108489 and Ppl128830), an intact laccase (Ppl89382), a truncated laccase model (Ppl46931), and the highly expressed FAD-dependent oxidoreductase Ppl114192 (Table 4). Gray bars and the left axis represent log2 microarray signals. Blackened bars and the right axis represent cDNA as determined by competitive RT-PCR. Asterisks indicate protein models whose peptides were identified in concentrated filtrates of aspen-grown cultures.

Tables

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  • TABLE 1.

    Gene expression summary for P. chrysosporium and P. placenta after 5 days of growth in medium containing ball-milled aspen as sole carbon source

    FeatureNo. of genes identified
    P. chrysosporiumP. placenta
    Gene modelsa10,04817,173 (12,227)
    Microarray target genes10,00412,438
    Proteins by LC-MS/MS7367
    Transcript and/or extracellular proteins accumulating in aspen culturesb
        Total77160
        Glycoside hydrolases3333
        Hypotheticals1549
        Oxidoreductases421
    • ↵ a Based on gene predictions previously described (36, 37, 53). The parenthetical number refers to the predicted number of unique alleles within the parental dikaryon strain of P. placenta.

    • ↵ b Number of genes whose transcripts accumulated >2-fold (P < .001) and/or whose predicted peptides were identified with Mascot scores of >40.

  • TABLE 2.

    P. chrysosporium genes encoding putative oxidoreductases upregulated >2-fold in BMA medium relative to glucose medium or matched to MS/MS-derived peptide sequencesa

    Phanerochaete chrysosporiumPostia placenta
    ModelPutative functionSignal (log2) in:RatioP valueModelAllellePairwise alignmentSignal (log2) in:RatioP value
    GluBMA% IDScoreGluBMA
    11098 Cellobiose dehydrogenase12.3015.619.93<0.001None
    138350Acetoin dehydrogenase8.8210.834.01<0.00188413110831751,0358.378.330.970.521
    6771Oxidoreductase10.0911.713.090.001604960561601761,54410.0711.412.53<0.001
    41616Aldo/keto reductase10.3711.932.960.00406None
    147Cytochrome b562 + CBM112.2213.622.64<0.001None
    10221Alcohol dehydrogenase10.7312.112.600.01050None
    10957Peroxidase LiPA9.5810.922.540.02240None
    121806Peroxidase LiPH10.9512.202.380.00352None
    1139FRE-like iron reductase12.6513.882.350.00331130043130030366359.9010.171.200.0349
    38849P45011.7212.882.24<0.001None
    126879 Alcohol oxidase*13.7714.741.970.02011872312984188309011.7614.446.43<0.001
    124398 Catalase*14.2414.901.590.00411472012316973200514.2714.331.040.526
    140211 Formate dehydrogenase*13.0413.531.410.110119730None85162812.6514.172.86<0.001
    6270Oxidoreductase (GMC)*9.8010.161.290.184None
    • ↵ a To identify conserved sequences, the 12,438 P. placenta protein models represented on microarrays were aligned with all 10,048 v2 P. chrysosporium protein models using Timelogic harware (Active Motif, Carlsbad, CA) with accelerated double affine Smith-Waterman alignments. Scores, percent identities, and related alignment parameters for all genes are listed in Table S1 of the supplemental material. Normalized microarray data are presented as the average log2 signal strength of three fully replicated experiments. Array-wide averaged signals (± standard deviations) for P. chrysosporium and P. placenta were 11.6 (1.6) and 10.9 (1.7), respectively. Significant accumulation (ratio) of transcripts in BMA relative to glucose (Glu) cultures was determined using the moderated t test (48) and associated false detection rates (4). Data are ranked according to the ratio, from highest to lowest. Underlined P. chrysosporium models correspond to genes with >50 cDNA tags in medium containing powdered oak (43). *, gene model whose proteins were identified in BMA filtrates by MS/MS. Table S1 in the supplemental material provides a summary of these data, and the complete MS/MS results are provided in Table S2.

  • TABLE 3.

    P. placenta genes encoding putative GHs with the highest transcript levels and/or positive MS/MS identification in BMA mediuma

    Postia placentaPhanerochaete chrysosporium
    ModelPutative functionAlleleSignal (log2) in:RatioP valueModelSignal (log2) in:RatioP value
    GluBMAGluBMA
    115648GH5 endo-1,4-β-glucanase*10896214.6215.041.330.0012 6458 12.1414.836.46<0.001
    119525GH18 glycosidase12096014.8114.831.020.75601372379.009.711.640.0060
    121831GH5 endo-β-1,4-mannosidase*13477213.4614.652.28<0.001 140501 9.0412.8914.44<0.001
    112941GH16 endo-1,3(4)-β-glucanase*6180912.6614.583.79<0.0011083311.7713.653.680.0019
    121713GH5 glucan 1,3-β-glucosidase4607712.7314.533.48<0.00112177410.1411.632.800.0092
    117860GH72 1,3-β-glucanosyltransferase*11895014.2914.511.160.0206643313.8313.330.710.0232
    134790GH27 α-galactosidase*9866212.7314.353.08<0.00113400111.6813.894.64<0.001
    94557GH51 α-N-arabinofuranosidase*None13.0614.312.38<0.001 3651 12.2012.961.700.0017
    127993GH35 β-galactosidase*12810113.6514.171.430.0033946611.2611.691.340.0709
    116267GH55 glucan 1,3-β-glucosidase*10864813.3514.161.75<0.001 8072 12.0313.983.880.0832
    100251GH51 α-N-arabinofuranosidase*12704612.3114.053.34<0.001365112.2012.961.700.00169
    134924GH31 α-glucosidase*9387813.3313.511.130.031612546212.3812.621.180.373
    113670GH10 endo-1,4-β-xylanase*13478712.6213.361.67<0.00113871511.1613.545.20<0.001
    57564GH2 β-mannosidase*5657612.3213.352.05<0.00113538513.3713.571.150.118
    126692GH79 glycosidase*11133211.7113.343.10<0.001199910.5511.882.520.0269
    97540GH37 trehalase*11592913.1113.141.020.677014062713.9612.800.450.0254
    112047GH92 α-1,2-mannosidase*11699213.1912.980.860.0134343112.7713.251.390.0109
    126595GH18 chitinase*13492312.5912.861.210.16303987214.0213.710.810.172
    112369GH20 β-hexosaminidase*6133112.9212.790.910.1450375229.059.081.020.781
    117345GH15 glucoamylase*11311212.3412.661.250.042013881312.4313.021.510.0771
    120395GH27 α-galactosidase*None11.5012.542.06<0.00112503312.2212.911.610.0193
    115593GH47 Man(9)-α-mannosidase*13492513.4812.510.51<0.001455011.6213.443.52<0.001
    110809GH43 galactan 1,3-β-galactosidase*None10.7512.503.38<0.00129710.6411.101.380.0625
    116199GH5 glucan 1,3- β-glucosidase*12842512.1512.471.240.0066222012.4313.662.350.00274
    111730GH28 polygalacturonase*4318910.5312.403.66<0.001 3805 10.9014.5712.70<0.001
    54405GH16 endo-1,3(4)-β-glucanase*13502011.3012.191.86<0.001 123909 12.3313.271.930.0283
    127469GH3 possible β-xylosidase*5121311.5812.081.420.0047 9257 9.2412.6710.79<0.001
    107557GH3 β-glucosidase*None11.9512.021.060.500013906314.7014.550.900.599
    46915GH3 β-glucosidase*9567711.0811.931.81<0.00112984911.2612.913.13<0.001
    105534GH10 endo-1,4-β-xylanase*None8.3811.7110.06<0.0011383459.2310.432.290.014
    55086GH31 α-glucosidase*1956410.9611.631.590.001496811.6412.732.120.0374
    52194GH13 α-amylase*9288111.4511.621.130.13603835713.8613.600.830.141
    62385GH92 α-1,2-mannosidase*4871611.3010.900.760.027813358512.0413.753.28<0.001
    130398GH20 β-hexosaminidase*13490710.159.880.830.005214058713.2913.491.150.233
    127046GH51 α-N-arabinofuranosidase*1002519.509.811.240.0053365112.2012.961.700.00169
    95568GH5 endo-1,4-β-mannosidase*None8.919.521.52<0.001657912.4313.672.360.00279
    • ↵ a Calculations are essentially the same as described for Table 2. The genes or alleles are listed in order of decreasing transcript levels. Detailed scores, e-values, and alignment parameters for the best P. chrysosporium hits are listed in Table S1 of the supplemental material. *, detection of peptides by LC-MS/MS in BMA medium filtrate (see Tables S1 and S2). Underlined P. chrysosporium models correspond to genes with >50 cDNA tags in medium containing powdered oak (43). Data are ranked according to P. placenta log2 signals in BMA. The first eight genes exceeded the genome-wide average signal by 2 standard deviations (>14.24). Questionable GH51 models Ppl9457 and Ppl127046 lie within a 10-kb region of scaffold 110, and alignments suggest possible duplication or assembly error. The 3′ termini of P. placenta models GH20 Ppl130398 and GH10 Ppl113670 are problematic and require additional data and manual annotation. However, MS/MS protein assignments are based on reliable (5′) regions of these models.

  • TABLE 4.

    P. placenta genes encoding putative oxidoreductases upregulated >2-fold in BMA medium relative to glucose medium or matched to MS/MS-derived peptide sequencesa

    Postia placentaPhanerochete chrysosporium
    ModelPutative functionAlleleSignal (log2) in:RatioP valueModelPairwise alignmentSignal (log2) in:RatioP value
    GluBMA% IDScoreGluBMA
    109824Ferroxidase Fet313462410.0112.726.55<0.0012689068227514.4012.950.370.0124
    107061Oxidoreductase510169.9012.616.54<0.00113817461112610.0710.141.050.698
    114245Polyphenol oxidase10929110.6213.326.48<0.001None
    118723Alcohol oxidase12984111.7614.446.43<0.001 126879 88309013.7714.741.970.0199
    1245171,4-Benzoquinone reductase640698.4111.026.10<0.00110307748219.7710.051.210.11
    34850Hydroquinol 1,2-dioxygenase876459.8612.215.09<0.001413307194311.2012.021.770.0252
    111395Short chain dehydrogenase645588.9511.154.60<0.00152587840410.6311.121.400.0162
    98518Formate dehydrogenase8989710.1212.033.76<0.001 140211 82157813.0413.531.410.106
    61437Aldehyde dehydrogenase892528.7510.573.51<0.0011339243348312.2511.030.430.0143
    46931Laccase (fragment)11131410.011.653.150.00710581402068.68.671.050.45
    1089892-Nitropropane dioxygenaseNone11.6013.203.04<0.00121875141211.9812.121.100.258
    113908Acireductone dioxygenase6361110.5112.113.03<0.0011238805350812.9012.820.940.491
    24981Hydroquinol 1,2-dioxygenase10788111.6013.132.88<0.0011366607998411.3411.891.460.0769
    119730Formate dehydrogenaseNone12.6514.172.86<0.001 140211 85162813.0413.531.410.106
    51235P450*2038511.7313.222.81<0.001120055135511.4011.511.080.38
    43234α-Aminoadipate reductaseNone10.8312.292.75<0.0016025298519.489.521.030.605
    61079Chloroperoxidase253918.9710.422.72<0.00132746392211.0711.371.230.0271
    116179Short chain dehydrogenaseNone11.2212.572.55<0.001132770699569.7110.051.270.0673
    49605Galacturonic acid reductase6160110.0711.412.53<0.001677176154410.0911.713.090.0016
    115028Aryl alcohol dehydrogenase8934311.5612.692.18<0.00112810371145910.4510.911.380.00751
    1083582-Nitropropane dioxygenase5679310.0111.082.11<0.001443287148610.8911.161.210.0874
    126817Flavin monooxygenase10488310.5411.622.110.008629157182511.8712.061.140.47
    111823Oxidoreductase12022512.6713.712.05<0.00122846813058.498.831.260.036
    56703CRO5*9963212.7313.601.820.0022888266365112.7212.550.890.277
    122772OR FAD linked*11419213.2214.071.80<0.0011380765311518.938.850.950.527
    128830Glucose oxidase-like*None13.2513.110.910.39101319613173412.3212.200.930.349
    • ↵ a Calculations are essentially the same as described for Table 2. The P. chrysosporium homolog with the highest alignment score was reported for each P. placenta gene. Scores, percent identity, and related alignment parameters for all genes are listed in Table S1 of the supplemental material. With one exception (galacturonic acid reductase), transcripts of the corresponding P. chrysosporium gene exhibited relatively lower accumulation ratios and a concomitantly higher false discovery rate (4) probability (far right column). Underlined P. chrysosporium models correspond to genes with >50 cDNA tags in medium containing powdered oak (43). Data are ranked according to the P. placenta ratio, from highest to lowest. *, detection of corresponding peptides by MS/MS in BMA medium filtrate.

Additional Files

  • Figures
  • Tables
  • Supplemental material

    Files in this Data Supplement:

    • Supplemental file 1 - Postia placenta protein models matched to best-hit Phanerochaete chrysosporium models (Table S1).
      Zipped Microsoft Excel file, 2.5 MB.
    • Supplemental file 2 - Detailed mass spectrometry results for Phanerochaete chrysosporium and Postia placenta (Table S2).
      Zipped Microsoft Excel file, 40K.
    • Supplemental file 3 - Primers and predicted lengths of Postia placenta genes analyzed by qRT-PCR (Table S3).
      Zipped Microsoft Excel file, 5K.
    • Supplemental file 4 - Scatter plots showing average log2 transcript levels for Phanerochaete chrysosporium and Postia placenta genes during growth on media containing ball-milled aspen or glucose as the sole carbon source (Fig. S1).
      Microsoft PowerPoint file, 1.3 MB.
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Comparative Transcriptome and Secretome Analysis of Wood Decay Fungi Postia placenta and Phanerochaete chrysosporium
Amber Vanden Wymelenberg, Jill Gaskell, Michael Mozuch, Grzegorz Sabat, John Ralph, Oleksandr Skyba, Shawn D. Mansfield, Robert A. Blanchette, Diego Martinez, Igor Grigoriev, Philip J. Kersten, Dan Cullen
Applied and Environmental Microbiology May 2010, 76 (11) 3599-3610; DOI: 10.1128/AEM.00058-10

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Comparative Transcriptome and Secretome Analysis of Wood Decay Fungi Postia placenta and Phanerochaete chrysosporium
Amber Vanden Wymelenberg, Jill Gaskell, Michael Mozuch, Grzegorz Sabat, John Ralph, Oleksandr Skyba, Shawn D. Mansfield, Robert A. Blanchette, Diego Martinez, Igor Grigoriev, Philip J. Kersten, Dan Cullen
Applied and Environmental Microbiology May 2010, 76 (11) 3599-3610; DOI: 10.1128/AEM.00058-10
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KEYWORDS

Coriolaceae
Fungal Proteins
Gene Expression Profiling
Phanerochaete
proteome
Wood

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