Genes associated with lignin degradation in the polyphagous white-rot pathogen Heterobasidion irregulare show substrate-specific regulation

Igor A. Yakovlev, Ari M. Hietala, Pierre-Emmanuel Courty, Taina Lundell, Halvor Solheim, Carl Gunnar Fossdal

Research output: Contribution to journalArticleScientificpeer-review

Abstract

The pathogenic white-rot basidiomycete Heterobasidion irregulare is able to remove lignin and hemicellulose prior to cellulose during the colonization of root and stem xylem of conifer and broadleaf trees. We identified and followed the regulation of expression of genes belonging to families encoding ligninolytic enzymes. In comparison with typical white-rot fungi, the H. irregulare genome has exclusively the short-manganese peroxidase type encoding genes (6 short-MnPs) and thereby a slight contraction in the pool of class II heme-containing peroxidases, but an expansion of the MCO laccases with 17 gene models. Furthermore, the genome shows a versatile set of other oxidoreductase genes putatively involved in lignin oxidation and conversion, including 5 glyoxal oxidases, 19 quinone-oxidoreductases and 12 aryl-alcohol oxidases. Their genetic multiplicity and gene-specific regulation patterns on cultures based on defined lignin, cellulose or Norway spruce lignocellulose substrates suggest divergent specificities and physiological roles for these enzymes. While the short-MnP encoding genes showed similar transcript levels upon fungal growth on heartwood and reaction zone (RZ), a xylem defense tissue rich in phenolic compounds unique to trees, a subset of laccases showed higher gene expression in the RZ cultures. In contrast, other oxidoreductases depending on initial MnP activity showed generally lower transcript levels on RZ than on heartwood. These data suggest that the rate of fungal oxidative conversion of xylem lignin differs between spruce RZ and heartwood. It is conceivable that in RZ part of the oxidoreductase activities of laccases are related to the detoxification of phenolic compounds involved in host-defense. Expression of the several short-MnP enzymes indicated an important role for these enzymes in effective delignification of wood by H. irregulare.

Original languageEnglish
JournalFungal Genetics and Biology
Volume56
Pages (from-to)17-24
Number of pages8
ISSN1087-1845
DOIs
Publication statusPublished - 2013
MoE publication typeA1 Journal article-refereed

Fields of Science

  • 1183 Plant biology, microbiology, virology
  • LIGNIN DEGRADATION
  • Wood decay fungi
  • Forest tree pathogen
  • Class II fungal secreted peroxidase
  • Heme peroxidase
  • Laccase
  • Multicopper oxidase
  • Hydrogen peroxide producing enzymes
  • 1184 Genetics, developmental biology, physiology
  • GENOMICS
  • transcriptomics
  • GENE EXPRESSION

Cite this

Yakovlev, Igor A. ; Hietala, Ari M. ; Courty, Pierre-Emmanuel ; Lundell, Taina ; Solheim, Halvor ; Fossdal, Carl Gunnar. / Genes associated with lignin degradation in the polyphagous white-rot pathogen Heterobasidion irregulare show substrate-specific regulation. In: Fungal Genetics and Biology. 2013 ; Vol. 56. pp. 17-24.
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title = "Genes associated with lignin degradation in the polyphagous white-rot pathogen Heterobasidion irregulare show substrate-specific regulation",
abstract = "The pathogenic white-rot basidiomycete Heterobasidion irregulare is able to remove lignin and hemicellulose prior to cellulose during the colonization of root and stem xylem of conifer and broadleaf trees. We identified and followed the regulation of expression of genes belonging to families encoding ligninolytic enzymes. In comparison with typical white-rot fungi, the H. irregulare genome has exclusively the short-manganese peroxidase type encoding genes (6 short-MnPs) and thereby a slight contraction in the pool of class II heme-containing peroxidases, but an expansion of the MCO laccases with 17 gene models. Furthermore, the genome shows a versatile set of other oxidoreductase genes putatively involved in lignin oxidation and conversion, including 5 glyoxal oxidases, 19 quinone-oxidoreductases and 12 aryl-alcohol oxidases. Their genetic multiplicity and gene-specific regulation patterns on cultures based on defined lignin, cellulose or Norway spruce lignocellulose substrates suggest divergent specificities and physiological roles for these enzymes. While the short-MnP encoding genes showed similar transcript levels upon fungal growth on heartwood and reaction zone (RZ), a xylem defense tissue rich in phenolic compounds unique to trees, a subset of laccases showed higher gene expression in the RZ cultures. In contrast, other oxidoreductases depending on initial MnP activity showed generally lower transcript levels on RZ than on heartwood. These data suggest that the rate of fungal oxidative conversion of xylem lignin differs between spruce RZ and heartwood. It is conceivable that in RZ part of the oxidoreductase activities of laccases are related to the detoxification of phenolic compounds involved in host-defense. Expression of the several short-MnP enzymes indicated an important role for these enzymes in effective delignification of wood by H. irregulare.",
keywords = "1183 Plant biology, microbiology, virology, LIGNIN DEGRADATION, Wood decay fungi, Forest tree pathogen, Class II fungal secreted peroxidase, Heme peroxidase, Laccase, Multicopper oxidase, Hydrogen peroxide producing enzymes, 1184 Genetics, developmental biology, physiology, GENOMICS, transcriptomics, GENE EXPRESSION",
author = "Yakovlev, {Igor A.} and Hietala, {Ari M.} and Pierre-Emmanuel Courty and Taina Lundell and Halvor Solheim and Fossdal, {Carl Gunnar}",
year = "2013",
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language = "English",
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pages = "17--24",
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Genes associated with lignin degradation in the polyphagous white-rot pathogen Heterobasidion irregulare show substrate-specific regulation. / Yakovlev, Igor A.; Hietala, Ari M.; Courty, Pierre-Emmanuel; Lundell, Taina; Solheim, Halvor; Fossdal, Carl Gunnar.

In: Fungal Genetics and Biology, Vol. 56, 2013, p. 17-24.

Research output: Contribution to journalArticleScientificpeer-review

TY - JOUR

T1 - Genes associated with lignin degradation in the polyphagous white-rot pathogen Heterobasidion irregulare show substrate-specific regulation

AU - Yakovlev, Igor A.

AU - Hietala, Ari M.

AU - Courty, Pierre-Emmanuel

AU - Lundell, Taina

AU - Solheim, Halvor

AU - Fossdal, Carl Gunnar

PY - 2013

Y1 - 2013

N2 - The pathogenic white-rot basidiomycete Heterobasidion irregulare is able to remove lignin and hemicellulose prior to cellulose during the colonization of root and stem xylem of conifer and broadleaf trees. We identified and followed the regulation of expression of genes belonging to families encoding ligninolytic enzymes. In comparison with typical white-rot fungi, the H. irregulare genome has exclusively the short-manganese peroxidase type encoding genes (6 short-MnPs) and thereby a slight contraction in the pool of class II heme-containing peroxidases, but an expansion of the MCO laccases with 17 gene models. Furthermore, the genome shows a versatile set of other oxidoreductase genes putatively involved in lignin oxidation and conversion, including 5 glyoxal oxidases, 19 quinone-oxidoreductases and 12 aryl-alcohol oxidases. Their genetic multiplicity and gene-specific regulation patterns on cultures based on defined lignin, cellulose or Norway spruce lignocellulose substrates suggest divergent specificities and physiological roles for these enzymes. While the short-MnP encoding genes showed similar transcript levels upon fungal growth on heartwood and reaction zone (RZ), a xylem defense tissue rich in phenolic compounds unique to trees, a subset of laccases showed higher gene expression in the RZ cultures. In contrast, other oxidoreductases depending on initial MnP activity showed generally lower transcript levels on RZ than on heartwood. These data suggest that the rate of fungal oxidative conversion of xylem lignin differs between spruce RZ and heartwood. It is conceivable that in RZ part of the oxidoreductase activities of laccases are related to the detoxification of phenolic compounds involved in host-defense. Expression of the several short-MnP enzymes indicated an important role for these enzymes in effective delignification of wood by H. irregulare.

AB - The pathogenic white-rot basidiomycete Heterobasidion irregulare is able to remove lignin and hemicellulose prior to cellulose during the colonization of root and stem xylem of conifer and broadleaf trees. We identified and followed the regulation of expression of genes belonging to families encoding ligninolytic enzymes. In comparison with typical white-rot fungi, the H. irregulare genome has exclusively the short-manganese peroxidase type encoding genes (6 short-MnPs) and thereby a slight contraction in the pool of class II heme-containing peroxidases, but an expansion of the MCO laccases with 17 gene models. Furthermore, the genome shows a versatile set of other oxidoreductase genes putatively involved in lignin oxidation and conversion, including 5 glyoxal oxidases, 19 quinone-oxidoreductases and 12 aryl-alcohol oxidases. Their genetic multiplicity and gene-specific regulation patterns on cultures based on defined lignin, cellulose or Norway spruce lignocellulose substrates suggest divergent specificities and physiological roles for these enzymes. While the short-MnP encoding genes showed similar transcript levels upon fungal growth on heartwood and reaction zone (RZ), a xylem defense tissue rich in phenolic compounds unique to trees, a subset of laccases showed higher gene expression in the RZ cultures. In contrast, other oxidoreductases depending on initial MnP activity showed generally lower transcript levels on RZ than on heartwood. These data suggest that the rate of fungal oxidative conversion of xylem lignin differs between spruce RZ and heartwood. It is conceivable that in RZ part of the oxidoreductase activities of laccases are related to the detoxification of phenolic compounds involved in host-defense. Expression of the several short-MnP enzymes indicated an important role for these enzymes in effective delignification of wood by H. irregulare.

KW - 1183 Plant biology, microbiology, virology

KW - LIGNIN DEGRADATION

KW - Wood decay fungi

KW - Forest tree pathogen

KW - Class II fungal secreted peroxidase

KW - Heme peroxidase

KW - Laccase

KW - Multicopper oxidase

KW - Hydrogen peroxide producing enzymes

KW - 1184 Genetics, developmental biology, physiology

KW - GENOMICS

KW - transcriptomics

KW - GENE EXPRESSION

U2 - 10.1016/j.fgb.2013.04.011

DO - 10.1016/j.fgb.2013.04.011

M3 - Article

VL - 56

SP - 17

EP - 24

JO - Fungal Genetics and Biology

JF - Fungal Genetics and Biology

SN - 1087-1845

ER -