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Analysis of the Phlebiopsis gigantea genome, transcriptome and secretome provides insight into its pioneer colonization strategies of wood.

Hori C, Ishida T, Igarashi K, Samejima M, Suzuki H, Master E, Ferreira P, Ruiz-Dueñas FJ, Held B, Canessa P, Larrondo LF, Schmoll M, Druzhinina IS, Kubicek CP, Gaskell JA, Kersten P, St John F, Glasner J, Sabat G, Splinter BonDurant S, Syed K, Yadav J, Mgbeahuruike AC, Kovalchuk A, Asiegbu FO, Lackner G, Hoffmeister D, Rencoret J, Gutiérrez A, Sun H, Lindquist E, Barry K, Riley R, Grigoriev IV, Henrissat B, Kües U, Berka RM, Martínez AT, Covert SF, Blanchette RA, Cullen D - PLoS Genet. (2014)

Bottom Line: Their products included an ABC transporter, lipases, cytochrome P450s, glutathione S-transferase and aldehyde dehydrogenase.Other regulated genes of unknown function and several constitutively expressed genes are also likely involved in P. gigantea's extractives metabolism.These results contribute to our fundamental understanding of pioneer colonization of conifer wood and provide insight into the diverse chemistries employed by fungi in carbon cycling processes.

View Article: PubMed Central - PubMed

Affiliation: Department of Biomaterials Sciences, University of Tokyo, Tokyo, Japan.

ABSTRACT
Collectively classified as white-rot fungi, certain basidiomycetes efficiently degrade the major structural polymers of wood cell walls. A small subset of these Agaricomycetes, exemplified by Phlebiopsis gigantea, is capable of colonizing freshly exposed conifer sapwood despite its high content of extractives, which retards the establishment of other fungal species. The mechanism(s) by which P. gigantea tolerates and metabolizes resinous compounds have not been explored. Here, we report the annotated P. gigantea genome and compare profiles of its transcriptome and secretome when cultured on fresh-cut versus solvent-extracted loblolly pine wood. The P. gigantea genome contains a conventional repertoire of hydrolase genes involved in cellulose/hemicellulose degradation, whose patterns of expression were relatively unperturbed by the absence of extractives. The expression of genes typically ascribed to lignin degradation was also largely unaffected. In contrast, genes likely involved in the transformation and detoxification of wood extractives were highly induced in its presence. Their products included an ABC transporter, lipases, cytochrome P450s, glutathione S-transferase and aldehyde dehydrogenase. Other regulated genes of unknown function and several constitutively expressed genes are also likely involved in P. gigantea's extractives metabolism. These results contribute to our fundamental understanding of pioneer colonization of conifer wood and provide insight into the diverse chemistries employed by fungi in carbon cycling processes.

No MeSH data available.


Related in: MedlinePlus

Comparative analysis of gene repertoires associated with degradation of plant cell wall polymers and extractives in 21 fungal genomes.(A) Principal component analysis (PCA) of 21 fungi using 73 CAZy and 12 AA families (Dataset S1). GMC oxidoreductases methanol oxidase, glucose oxidase and aryl alcohol oxidase were excluded because confident functional assignments could not be made and/or their inclusion did not contribute to separation of white- and brown-rot species. (B) PCA of 21 fungi using genes encoding 14 enzymes involved in lipid metabolism (KEGG reference pathway 00071, Dataset S1). There is no significant segregation of white-rot and brown-rot fungi although P. gigantea was positioned in the third quadrant with B. adusta and P. carnosa. Symbols for white rot and brown rot fungi appear in blue and red, respectively. Tremella mesenterica is a mycoparasite. For raw data and contributions of the top 20 families see Dataset S1, Text S1 and Figures S2 and S3.
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pgen-1004759-g003: Comparative analysis of gene repertoires associated with degradation of plant cell wall polymers and extractives in 21 fungal genomes.(A) Principal component analysis (PCA) of 21 fungi using 73 CAZy and 12 AA families (Dataset S1). GMC oxidoreductases methanol oxidase, glucose oxidase and aryl alcohol oxidase were excluded because confident functional assignments could not be made and/or their inclusion did not contribute to separation of white- and brown-rot species. (B) PCA of 21 fungi using genes encoding 14 enzymes involved in lipid metabolism (KEGG reference pathway 00071, Dataset S1). There is no significant segregation of white-rot and brown-rot fungi although P. gigantea was positioned in the third quadrant with B. adusta and P. carnosa. Symbols for white rot and brown rot fungi appear in blue and red, respectively. Tremella mesenterica is a mycoparasite. For raw data and contributions of the top 20 families see Dataset S1, Text S1 and Figures S2 and S3.

Mentions: Principal component analysis (PCA), based on 73 and 12 families of carbohydrate active enzymes (CAZys, [16]) and auxiliary activities (AAs), [30]), respectively, clustered P. gigantea with other efficient lignin degraders ([39], Figures 3A and S2). Gene numbers were extracted from 21 fungal genomes and excluded genes encoding putative GMC oxidases such as methanol oxidase, alcohol oxidase and glucose oxidase (Dataset S1). Highest contribution of PC1 (50% of variance separating white-rot and brown-rot fungi) and PC2 (13.0% of variance)) values were those genes associated with degradation of plant cell wall polysaccharides and lignin, respectively (Text S1). Hierarchical clustering analysis with this dataset also categorized P. gigantea into a clade of white-rot fungi that included the polypore P. chrysosporium. The precise number and distribution of P. gigantea genes likely involved in lignocellulose degradation were similar, but not identical, to other polypores such as P. chrysosporium and C. subvermispora (Figure 4). Like P. chrysosporium and Phanerochaete flavido-alba, P. gigantea had no laccase sensu stricto genes. Interestingly, while both P. gigantea and the white-rot Russulales H. annosum are adapted to colonization of conifers, significant numbers of laccase sensu stricto genes were only observed in H. annosum (Figure 4). This important conifer pathogen also lacked GLX, LiP and representatives of GH5 subfamiles 15 and 31.


Analysis of the Phlebiopsis gigantea genome, transcriptome and secretome provides insight into its pioneer colonization strategies of wood.

Hori C, Ishida T, Igarashi K, Samejima M, Suzuki H, Master E, Ferreira P, Ruiz-Dueñas FJ, Held B, Canessa P, Larrondo LF, Schmoll M, Druzhinina IS, Kubicek CP, Gaskell JA, Kersten P, St John F, Glasner J, Sabat G, Splinter BonDurant S, Syed K, Yadav J, Mgbeahuruike AC, Kovalchuk A, Asiegbu FO, Lackner G, Hoffmeister D, Rencoret J, Gutiérrez A, Sun H, Lindquist E, Barry K, Riley R, Grigoriev IV, Henrissat B, Kües U, Berka RM, Martínez AT, Covert SF, Blanchette RA, Cullen D - PLoS Genet. (2014)

Comparative analysis of gene repertoires associated with degradation of plant cell wall polymers and extractives in 21 fungal genomes.(A) Principal component analysis (PCA) of 21 fungi using 73 CAZy and 12 AA families (Dataset S1). GMC oxidoreductases methanol oxidase, glucose oxidase and aryl alcohol oxidase were excluded because confident functional assignments could not be made and/or their inclusion did not contribute to separation of white- and brown-rot species. (B) PCA of 21 fungi using genes encoding 14 enzymes involved in lipid metabolism (KEGG reference pathway 00071, Dataset S1). There is no significant segregation of white-rot and brown-rot fungi although P. gigantea was positioned in the third quadrant with B. adusta and P. carnosa. Symbols for white rot and brown rot fungi appear in blue and red, respectively. Tremella mesenterica is a mycoparasite. For raw data and contributions of the top 20 families see Dataset S1, Text S1 and Figures S2 and S3.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4256170&req=5

pgen-1004759-g003: Comparative analysis of gene repertoires associated with degradation of plant cell wall polymers and extractives in 21 fungal genomes.(A) Principal component analysis (PCA) of 21 fungi using 73 CAZy and 12 AA families (Dataset S1). GMC oxidoreductases methanol oxidase, glucose oxidase and aryl alcohol oxidase were excluded because confident functional assignments could not be made and/or their inclusion did not contribute to separation of white- and brown-rot species. (B) PCA of 21 fungi using genes encoding 14 enzymes involved in lipid metabolism (KEGG reference pathway 00071, Dataset S1). There is no significant segregation of white-rot and brown-rot fungi although P. gigantea was positioned in the third quadrant with B. adusta and P. carnosa. Symbols for white rot and brown rot fungi appear in blue and red, respectively. Tremella mesenterica is a mycoparasite. For raw data and contributions of the top 20 families see Dataset S1, Text S1 and Figures S2 and S3.
Mentions: Principal component analysis (PCA), based on 73 and 12 families of carbohydrate active enzymes (CAZys, [16]) and auxiliary activities (AAs), [30]), respectively, clustered P. gigantea with other efficient lignin degraders ([39], Figures 3A and S2). Gene numbers were extracted from 21 fungal genomes and excluded genes encoding putative GMC oxidases such as methanol oxidase, alcohol oxidase and glucose oxidase (Dataset S1). Highest contribution of PC1 (50% of variance separating white-rot and brown-rot fungi) and PC2 (13.0% of variance)) values were those genes associated with degradation of plant cell wall polysaccharides and lignin, respectively (Text S1). Hierarchical clustering analysis with this dataset also categorized P. gigantea into a clade of white-rot fungi that included the polypore P. chrysosporium. The precise number and distribution of P. gigantea genes likely involved in lignocellulose degradation were similar, but not identical, to other polypores such as P. chrysosporium and C. subvermispora (Figure 4). Like P. chrysosporium and Phanerochaete flavido-alba, P. gigantea had no laccase sensu stricto genes. Interestingly, while both P. gigantea and the white-rot Russulales H. annosum are adapted to colonization of conifers, significant numbers of laccase sensu stricto genes were only observed in H. annosum (Figure 4). This important conifer pathogen also lacked GLX, LiP and representatives of GH5 subfamiles 15 and 31.

Bottom Line: Their products included an ABC transporter, lipases, cytochrome P450s, glutathione S-transferase and aldehyde dehydrogenase.Other regulated genes of unknown function and several constitutively expressed genes are also likely involved in P. gigantea's extractives metabolism.These results contribute to our fundamental understanding of pioneer colonization of conifer wood and provide insight into the diverse chemistries employed by fungi in carbon cycling processes.

View Article: PubMed Central - PubMed

Affiliation: Department of Biomaterials Sciences, University of Tokyo, Tokyo, Japan.

ABSTRACT
Collectively classified as white-rot fungi, certain basidiomycetes efficiently degrade the major structural polymers of wood cell walls. A small subset of these Agaricomycetes, exemplified by Phlebiopsis gigantea, is capable of colonizing freshly exposed conifer sapwood despite its high content of extractives, which retards the establishment of other fungal species. The mechanism(s) by which P. gigantea tolerates and metabolizes resinous compounds have not been explored. Here, we report the annotated P. gigantea genome and compare profiles of its transcriptome and secretome when cultured on fresh-cut versus solvent-extracted loblolly pine wood. The P. gigantea genome contains a conventional repertoire of hydrolase genes involved in cellulose/hemicellulose degradation, whose patterns of expression were relatively unperturbed by the absence of extractives. The expression of genes typically ascribed to lignin degradation was also largely unaffected. In contrast, genes likely involved in the transformation and detoxification of wood extractives were highly induced in its presence. Their products included an ABC transporter, lipases, cytochrome P450s, glutathione S-transferase and aldehyde dehydrogenase. Other regulated genes of unknown function and several constitutively expressed genes are also likely involved in P. gigantea's extractives metabolism. These results contribute to our fundamental understanding of pioneer colonization of conifer wood and provide insight into the diverse chemistries employed by fungi in carbon cycling processes.

No MeSH data available.


Related in: MedlinePlus