Flavanone-3-Hydroxylase Plays an Important Role in the Biosynthesis of Spruce Phenolic Defenses Against Bark Beetles and Their Fungal Associates
Conifer forests worldwide are becoming increasingly vulnerable to attacks by bark beetles and their fungal associates due to the effects of global warming. Attack by the bark beetle Ips typographus and the blue-stain fungus it vectors (Endoconidiophora polonica) on Norway spruce (Picea abies) is wel...
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2019-02-01
|
| Series: | Frontiers in Plant Science |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/article/10.3389/fpls.2019.00208/full |
| _version_ | 1818931332732944384 |
|---|---|
| author | Almuth Hammerbacher Dineshkumar Kandasamy Chhana Ullah Axel Schmidt Louwrance P. Wright Jonathan Gershenzon |
| author_facet | Almuth Hammerbacher Dineshkumar Kandasamy Chhana Ullah Axel Schmidt Louwrance P. Wright Jonathan Gershenzon |
| author_sort | Almuth Hammerbacher |
| collection | DOAJ |
| description | Conifer forests worldwide are becoming increasingly vulnerable to attacks by bark beetles and their fungal associates due to the effects of global warming. Attack by the bark beetle Ips typographus and the blue-stain fungus it vectors (Endoconidiophora polonica) on Norway spruce (Picea abies) is well known to induce increased production of terpene oleoresin and polyphenolic compounds. However, it is not clear whether specific compounds are important in resisting attack. In this study, we observed a significant increase in dihydroflavonol and flavan-3-ol content after inoculating Norway spruce with the bark beetle vectored fungus. A bioassay revealed that the dihydroflavonol taxifolin and the flavan-3-ol catechin negatively affected both I. typographus and E. polonica. The biosynthesis of flavan-3-ols is well studied in Norway spruce, but little is known about dihydroflavonol formation in this species. A flavanone-3-hydroxylase (F3H) was identified that catalyzed the conversion of eriodictyol to taxifolin and was highly expressed after E. polonica infection. Down-regulating F3H gene expression by RNA interference in transgenic Norway spruce resulted in significantly lower levels of both dihydroflavonols and flavan-3-ols. Therefore F3H plays a key role in the biosynthesis of defense compounds in Norway spruce that act against the bark beetle-fungus complex. This enzyme forms a defensive product, taxifolin, which is also a metabolic precursor of another defensive product, catechin, which in turn synergizes the toxicity of taxifolin to the bark beetle associated fungus. |
| first_indexed | 2024-12-20T04:14:55Z |
| format | Article |
| id | doaj.art-bf943c6461c54eff9df57fe3b8e2c22e |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-12-20T04:14:55Z |
| publishDate | 2019-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-bf943c6461c54eff9df57fe3b8e2c22e2022-12-21T19:53:48ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2019-02-011010.3389/fpls.2019.00208422913Flavanone-3-Hydroxylase Plays an Important Role in the Biosynthesis of Spruce Phenolic Defenses Against Bark Beetles and Their Fungal AssociatesAlmuth Hammerbacher0Dineshkumar Kandasamy1Chhana Ullah2Axel Schmidt3Louwrance P. Wright4Jonathan Gershenzon5Department of Zoology and Entomology, Forestry and Agricultural Biotechnology Institute, University of Pretoria, Pretoria, South AfricaDepartment of Biochemistry, Max Planck Institute for Chemical Ecology, Jena, GermanyDepartment of Biochemistry, Max Planck Institute for Chemical Ecology, Jena, GermanyDepartment of Biochemistry, Max Planck Institute for Chemical Ecology, Jena, GermanyZeiselhof Research Farm, Pretoria, South AfricaDepartment of Biochemistry, Max Planck Institute for Chemical Ecology, Jena, GermanyConifer forests worldwide are becoming increasingly vulnerable to attacks by bark beetles and their fungal associates due to the effects of global warming. Attack by the bark beetle Ips typographus and the blue-stain fungus it vectors (Endoconidiophora polonica) on Norway spruce (Picea abies) is well known to induce increased production of terpene oleoresin and polyphenolic compounds. However, it is not clear whether specific compounds are important in resisting attack. In this study, we observed a significant increase in dihydroflavonol and flavan-3-ol content after inoculating Norway spruce with the bark beetle vectored fungus. A bioassay revealed that the dihydroflavonol taxifolin and the flavan-3-ol catechin negatively affected both I. typographus and E. polonica. The biosynthesis of flavan-3-ols is well studied in Norway spruce, but little is known about dihydroflavonol formation in this species. A flavanone-3-hydroxylase (F3H) was identified that catalyzed the conversion of eriodictyol to taxifolin and was highly expressed after E. polonica infection. Down-regulating F3H gene expression by RNA interference in transgenic Norway spruce resulted in significantly lower levels of both dihydroflavonols and flavan-3-ols. Therefore F3H plays a key role in the biosynthesis of defense compounds in Norway spruce that act against the bark beetle-fungus complex. This enzyme forms a defensive product, taxifolin, which is also a metabolic precursor of another defensive product, catechin, which in turn synergizes the toxicity of taxifolin to the bark beetle associated fungus.https://www.frontiersin.org/article/10.3389/fpls.2019.00208/fulltaxifolincatechinflavonoidsF3HPicea abiesEndoconidiophora polonica |
| spellingShingle | Almuth Hammerbacher Dineshkumar Kandasamy Chhana Ullah Axel Schmidt Louwrance P. Wright Jonathan Gershenzon Flavanone-3-Hydroxylase Plays an Important Role in the Biosynthesis of Spruce Phenolic Defenses Against Bark Beetles and Their Fungal Associates Frontiers in Plant Science taxifolin catechin flavonoids F3H Picea abies Endoconidiophora polonica |
| title | Flavanone-3-Hydroxylase Plays an Important Role in the Biosynthesis of Spruce Phenolic Defenses Against Bark Beetles and Their Fungal Associates |
| title_full | Flavanone-3-Hydroxylase Plays an Important Role in the Biosynthesis of Spruce Phenolic Defenses Against Bark Beetles and Their Fungal Associates |
| title_fullStr | Flavanone-3-Hydroxylase Plays an Important Role in the Biosynthesis of Spruce Phenolic Defenses Against Bark Beetles and Their Fungal Associates |
| title_full_unstemmed | Flavanone-3-Hydroxylase Plays an Important Role in the Biosynthesis of Spruce Phenolic Defenses Against Bark Beetles and Their Fungal Associates |
| title_short | Flavanone-3-Hydroxylase Plays an Important Role in the Biosynthesis of Spruce Phenolic Defenses Against Bark Beetles and Their Fungal Associates |
| title_sort | flavanone 3 hydroxylase plays an important role in the biosynthesis of spruce phenolic defenses against bark beetles and their fungal associates |
| topic | taxifolin catechin flavonoids F3H Picea abies Endoconidiophora polonica |
| url | https://www.frontiersin.org/article/10.3389/fpls.2019.00208/full |
| work_keys_str_mv | AT almuthhammerbacher flavanone3hydroxylaseplaysanimportantroleinthebiosynthesisofsprucephenolicdefensesagainstbarkbeetlesandtheirfungalassociates AT dineshkumarkandasamy flavanone3hydroxylaseplaysanimportantroleinthebiosynthesisofsprucephenolicdefensesagainstbarkbeetlesandtheirfungalassociates AT chhanaullah flavanone3hydroxylaseplaysanimportantroleinthebiosynthesisofsprucephenolicdefensesagainstbarkbeetlesandtheirfungalassociates AT axelschmidt flavanone3hydroxylaseplaysanimportantroleinthebiosynthesisofsprucephenolicdefensesagainstbarkbeetlesandtheirfungalassociates AT louwrancepwright flavanone3hydroxylaseplaysanimportantroleinthebiosynthesisofsprucephenolicdefensesagainstbarkbeetlesandtheirfungalassociates AT jonathangershenzon flavanone3hydroxylaseplaysanimportantroleinthebiosynthesisofsprucephenolicdefensesagainstbarkbeetlesandtheirfungalassociates |