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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

Glyoxalate shunt and proposed relationship to lipid oxidation when P. gigantea is cultivated on wood-containing media (ELP or NELP) relative to Glc medium.Enzymes encoded by upregulated genes are black highlighted and associated with thickened arrows. Abbreviations: ABC-G1, ABC transporter associated with monoterpene tolerance; ADH/AO, Acyl-CoA dehydrogenase/oxidase; AH, Aconitate hydratase; CoA ligase, long fatty acid-CoA ligase; DLAT, Dihydrolipoyllysine-residue acetyltransferase; DLST, Dihydrolipoyllysine-residue succinyltransferase; EH, Enoyl-CoA hydratase; FDH, Formate dehydrogenase; FH, Fumarate hydratase; KT, Ketothiolase (acetyl-CoA C-acyltransferase); HAD, 3-Hydroxyacyl-CoA dehydrogenase; ICL, Isocitrate lyase; IDH, Isocitrate dehydrogenase; MDH, Malate dehydrogenase; MS, Malate synthase; ODH, Oxoglutarate dehydrogenase; OXA, Oxaloacetase; OXDC, Oxalate decarboxylase; OXO, Oxalate oxidase; PC, Pyruvate carboxylase; PDH, Pyruvate dehydrogenase; PEP, Phosphoenolpyruvate; PEPCK, Phosphoenolpyruvate carboxykinase; PEPK, Phosphoenolpyruvate kinase; SDH, succinate dehydrogenase. See Dataset S2 for detailed gene expression data.
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pgen-1004759-g009: Glyoxalate shunt and proposed relationship to lipid oxidation when P. gigantea is cultivated on wood-containing media (ELP or NELP) relative to Glc medium.Enzymes encoded by upregulated genes are black highlighted and associated with thickened arrows. Abbreviations: ABC-G1, ABC transporter associated with monoterpene tolerance; ADH/AO, Acyl-CoA dehydrogenase/oxidase; AH, Aconitate hydratase; CoA ligase, long fatty acid-CoA ligase; DLAT, Dihydrolipoyllysine-residue acetyltransferase; DLST, Dihydrolipoyllysine-residue succinyltransferase; EH, Enoyl-CoA hydratase; FDH, Formate dehydrogenase; FH, Fumarate hydratase; KT, Ketothiolase (acetyl-CoA C-acyltransferase); HAD, 3-Hydroxyacyl-CoA dehydrogenase; ICL, Isocitrate lyase; IDH, Isocitrate dehydrogenase; MDH, Malate dehydrogenase; MS, Malate synthase; ODH, Oxoglutarate dehydrogenase; OXA, Oxaloacetase; OXDC, Oxalate decarboxylase; OXO, Oxalate oxidase; PC, Pyruvate carboxylase; PDH, Pyruvate dehydrogenase; PEP, Phosphoenolpyruvate; PEPCK, Phosphoenolpyruvate carboxykinase; PEPK, Phosphoenolpyruvate kinase; SDH, succinate dehydrogenase. See Dataset S2 for detailed gene expression data.

Mentions: To identify enzymes involved in tolerance to and/or degradation of extractives, comparisons were made of gene expression in ground loblolly pine wood that had been extensively extracted with acetone (ELP) versus non-extracted loblolly pine wood (NELP) (Figure 7A). In general, this treatment had little impact on gene expression. For example, glycoside hydrolase transcript and protein patterns showed only minor differences (Figure 8). Nevertheless, transcripts corresponding to 22 genes showed significantly increased levels (>4-fold; p<0.01) in NELP relative to ELP (Figure 7B; Table 2). Of particular interest were genes potentially involved in metabolism of resin acids (e.g. CYPs; [55]), in altering the accessibility of cell wall components (e.g., an endoxylanase), and in regulating gene expression (e.g. proteins containing putative Zn finger domains or HMG-Box transcription factors). Integration of transcript profiles of genes involved in intracellular lipid and oxalate metabolism, together with TCA and glyoxylate cycles, strongly supports a central role for β-oxidation in triglyceride and terpenoid transformation by P. gigantea (Figure 9).


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)

Glyoxalate shunt and proposed relationship to lipid oxidation when P. gigantea is cultivated on wood-containing media (ELP or NELP) relative to Glc medium.Enzymes encoded by upregulated genes are black highlighted and associated with thickened arrows. Abbreviations: ABC-G1, ABC transporter associated with monoterpene tolerance; ADH/AO, Acyl-CoA dehydrogenase/oxidase; AH, Aconitate hydratase; CoA ligase, long fatty acid-CoA ligase; DLAT, Dihydrolipoyllysine-residue acetyltransferase; DLST, Dihydrolipoyllysine-residue succinyltransferase; EH, Enoyl-CoA hydratase; FDH, Formate dehydrogenase; FH, Fumarate hydratase; KT, Ketothiolase (acetyl-CoA C-acyltransferase); HAD, 3-Hydroxyacyl-CoA dehydrogenase; ICL, Isocitrate lyase; IDH, Isocitrate dehydrogenase; MDH, Malate dehydrogenase; MS, Malate synthase; ODH, Oxoglutarate dehydrogenase; OXA, Oxaloacetase; OXDC, Oxalate decarboxylase; OXO, Oxalate oxidase; PC, Pyruvate carboxylase; PDH, Pyruvate dehydrogenase; PEP, Phosphoenolpyruvate; PEPCK, Phosphoenolpyruvate carboxykinase; PEPK, Phosphoenolpyruvate kinase; SDH, succinate dehydrogenase. See Dataset S2 for detailed gene expression data.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4256170&req=5

pgen-1004759-g009: Glyoxalate shunt and proposed relationship to lipid oxidation when P. gigantea is cultivated on wood-containing media (ELP or NELP) relative to Glc medium.Enzymes encoded by upregulated genes are black highlighted and associated with thickened arrows. Abbreviations: ABC-G1, ABC transporter associated with monoterpene tolerance; ADH/AO, Acyl-CoA dehydrogenase/oxidase; AH, Aconitate hydratase; CoA ligase, long fatty acid-CoA ligase; DLAT, Dihydrolipoyllysine-residue acetyltransferase; DLST, Dihydrolipoyllysine-residue succinyltransferase; EH, Enoyl-CoA hydratase; FDH, Formate dehydrogenase; FH, Fumarate hydratase; KT, Ketothiolase (acetyl-CoA C-acyltransferase); HAD, 3-Hydroxyacyl-CoA dehydrogenase; ICL, Isocitrate lyase; IDH, Isocitrate dehydrogenase; MDH, Malate dehydrogenase; MS, Malate synthase; ODH, Oxoglutarate dehydrogenase; OXA, Oxaloacetase; OXDC, Oxalate decarboxylase; OXO, Oxalate oxidase; PC, Pyruvate carboxylase; PDH, Pyruvate dehydrogenase; PEP, Phosphoenolpyruvate; PEPCK, Phosphoenolpyruvate carboxykinase; PEPK, Phosphoenolpyruvate kinase; SDH, succinate dehydrogenase. See Dataset S2 for detailed gene expression data.
Mentions: To identify enzymes involved in tolerance to and/or degradation of extractives, comparisons were made of gene expression in ground loblolly pine wood that had been extensively extracted with acetone (ELP) versus non-extracted loblolly pine wood (NELP) (Figure 7A). In general, this treatment had little impact on gene expression. For example, glycoside hydrolase transcript and protein patterns showed only minor differences (Figure 8). Nevertheless, transcripts corresponding to 22 genes showed significantly increased levels (>4-fold; p<0.01) in NELP relative to ELP (Figure 7B; Table 2). Of particular interest were genes potentially involved in metabolism of resin acids (e.g. CYPs; [55]), in altering the accessibility of cell wall components (e.g., an endoxylanase), and in regulating gene expression (e.g. proteins containing putative Zn finger domains or HMG-Box transcription factors). Integration of transcript profiles of genes involved in intracellular lipid and oxalate metabolism, together with TCA and glyoxylate cycles, strongly supports a central role for β-oxidation in triglyceride and terpenoid transformation by P. gigantea (Figure 9).

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