title: The Bark-Beetle-Associated Fungus, Endoconidiophora polonica, Utilizes the Phenolic Defense Compounds of Its Host as a Carbon Source.
abstract: Norway spruce (Picea abies) is periodically attacked by the bark beetle Ips typographus and its fungal associate, Endoconidiophora polonica, whose infection is thought to be required for successful beetle attack. Norway spruce produces terpenoid resins and phenolics in response to fungal and bark beetle invasion. However, how the fungal associate copes with these chemical defenses is still unclear. In this study, we investigated changes in the phenolic content of Norway spruce bark upon E. polonica infection and the biochemical factors mediating these changes. Although genes encoding the rate-limiting enzymes in Norway spruce stilbene and flavonoid biosynthesis were actively transcribed during fungal infection, there was a significant time-dependent decline of the corresponding metabolites in fungal lesions. In vitro feeding experiments with pure phenolics revealed that E. polonica transforms both stilbenes and flavonoids to muconoid-type ring-cleavage products, which are likely the first steps in the degradation of spruce defenses to substrates that can enter the tricarboxylic acid cycle. Four genes were identified in E. polonica that encode catechol dioxygenases carrying out these reactions. These enzymes catalyze the cleavage of phenolic rings with a vicinal dihydroxyl group to muconoid products accepting a wide range of Norway spruce-produced phenolics as substrates. The expression of these genes and E. polonica utilization of the most abundant spruce phenolics as carbon sources both correlated positively with fungal virulence in several strains. Thus, the pathways for the degradation of phenolic compounds in E. polonica, initiated by catechol dioxygenase action, are important to the infection, growth, and survival of this bark beetle-vectored fungus and may play a major role in the ability of I. typographus to colonize spruce trees.
authors.affiliation: Max Planck Institute for Chemical Ecology, 07745 Jena, Germany (N.W., D.K., H.V., C.P., L.P.W., J.G., A.H.);University of Potsdam, 14476 Golm, Germany (L.L.); andDepartment of Genetics, Forestry and Agricultural Biotechnology Institute, University of Pretoria, Pretoria 0028, South Africa (B.D.W.).
authors.forename: Namita
authors.initials: N
authors.lastname: Wadke
authors.affiliation: Max Planck Institute for Chemical Ecology, 07745 Jena, Germany (N.W., D.K., H.V., C.P., L.P.W., J.G., A.H.);University of Potsdam, 14476 Golm, Germany (L.L.); andDepartment of Genetics, Forestry and Agricultural Biotechnology Institute, University of Pretoria, Pretoria 0028, South Africa (B.D.W.).
authors.forename: Dineshkumar
authors.initials: D
authors.lastname: Kandasamy
authors.affiliation: Max Planck Institute for Chemical Ecology, 07745 Jena, Germany (N.W., D.K., H.V., C.P., L.P.W., J.G., A.H.);University of Potsdam, 14476 Golm, Germany (L.L.); andDepartment of Genetics, Forestry and Agricultural Biotechnology Institute, University of Pretoria, Pretoria 0028, South Africa (B.D.W.).
authors.forename: Heiko
authors.initials: H
authors.lastname: Vogel
authors.affiliation: Max Planck Institute for Chemical Ecology, 07745 Jena, Germany (N.W., D.K., H.V., C.P., L.P.W., J.G., A.H.);University of Potsdam, 14476 Golm, Germany (L.L.); andDepartment of Genetics, Forestry and Agricultural Biotechnology Institute, University of Pretoria, Pretoria 0028, South Africa (B.D.W.).
authors.forename: Ljerka
authors.identifier: 0000-0003-4988-6263
authors.initials: L
authors.lastname: Lah
authors.affiliation: Max Planck Institute for Chemical Ecology, 07745 Jena, Germany (N.W., D.K., H.V., C.P., L.P.W., J.G., A.H.);University of Potsdam, 14476 Golm, Germany (L.L.); andDepartment of Genetics, Forestry and Agricultural Biotechnology Institute, University of Pretoria, Pretoria 0028, South Africa (B.D.W.).
authors.forename: Brenda D
authors.initials: BD
authors.lastname: Wingfield
authors.affiliation: Max Planck Institute for Chemical Ecology, 07745 Jena, Germany (N.W., D.K., H.V., C.P., L.P.W., J.G., A.H.);University of Potsdam, 14476 Golm, Germany (L.L.); andDepartment of Genetics, Forestry and Agricultural Biotechnology Institute, University of Pretoria, Pretoria 0028, South Africa (B.D.W.).
authors.forename: Christian
authors.initials: C
authors.lastname: Paetz
authors.affiliation: Max Planck Institute for Chemical Ecology, 07745 Jena, Germany (N.W., D.K., H.V., C.P., L.P.W., J.G., A.H.);University of Potsdam, 14476 Golm, Germany (L.L.); andDepartment of Genetics, Forestry and Agricultural Biotechnology Institute, University of Pretoria, Pretoria 0028, South Africa (B.D.W.).
authors.forename: Louwrance P
authors.identifier: 0000-0001-5998-6079
authors.initials: LP
authors.lastname: Wright
authors.affiliation: Max Planck Institute for Chemical Ecology, 07745 Jena, Germany (N.W., D.K., H.V., C.P., L.P.W., J.G., A.H.);University of Potsdam, 14476 Golm, Germany (L.L.); andDepartment of Genetics, Forestry and Agricultural Biotechnology Institute, University of Pretoria, Pretoria 0028, South Africa (B.D.W.).
authors.forename: Jonathan
authors.identifier: 0000-0002-1812-1551
authors.initials: J
authors.lastname: Gershenzon
authors.affiliation: Max Planck Institute for Chemical Ecology, 07745 Jena, Germany (N.W., D.K., H.V., C.P., L.P.W., J.G., A.H.);University of Potsdam, 14476 Golm, Germany (L.L.); andDepartment of Genetics, Forestry and Agricultural Biotechnology Institute, University of Pretoria, Pretoria 0028, South Africa (B.D.W.) ahammerbacher@ice.mpg.de.
authors.forename: Almuth
authors.identifier: 0000-0002-0262-2634
authors.initials: A
authors.lastname: Hammerbacher
mesh_terms: D000818:Animals; D001203:Ascomycota / Q000472:pathogenicity / Q000502:physiology*; D002244:Carbon / Q000378:metabolism*; D050548:Catechol 1,2-Dioxygenase / Q000235:genetics / Q000378:metabolism; D002396:Catechols / Q000737:chemistry / Q000378:metabolism; D005419:Flavonoids / Q000737:chemistry / Q000378:metabolism; D010636:Phenols / Q000737:chemistry / Q000378:metabolism*; D028222:Picea / Q000737:chemistry / Q000382:microbiology*; D010935:Plant Diseases / Q000382:microbiology*; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism; D012116:Resins, Plant / Q000737:chemistry / Q000378:metabolism; D013267:Stilbenes / Q000737:chemistry / Q000378:metabolism; D013729:Terpenes / Q000737:chemistry / Q000378:metabolism; D037521:Virulence Factors; D048889:Weevils / Q000382:microbiology*
chemical_list: D002396:Catechols; D005419:Flavonoids; D010636:Phenols; D010940:Plant Proteins; D012116:Resins, Plant; D013267:Stilbenes; D013729:Terpenes; D037521:Virulence Factors; D002244:Carbon; D050548:Catechol 1,2-Dioxygenase; C034221:catechol