Patterns and roles of lignan and terpenoid accumulation in the reaction zone compartmentalizing pathogen-infected heartwood of Norway spruce

MAIN CONCLUSION: Lignan impregnation of the reaction zone wood protects against oxidative degradation by fungi. Traumatic resin canals may play roles in the underlying signal transduction, synthesis, and translocation of defense compounds. ABSTRACT: Tree defense against xylem pathogens involves both...

Descripción completa

Detalles Bibliográficos
Autores principales: Nagy, Nina Elisabeth, Norli, Hans Ragnar, Fongen, Monica, Østby, Runa Berg, Heldal, Inger M., Davik, Jahn, Hietala, Ari M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer Berlin Heidelberg 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8831285/
https://www.ncbi.nlm.nih.gov/pubmed/35142905
http://dx.doi.org/10.1007/s00425-022-03842-1
_version_ 1784648472410980352
author Nagy, Nina Elisabeth
Norli, Hans Ragnar
Fongen, Monica
Østby, Runa Berg
Heldal, Inger M.
Davik, Jahn
Hietala, Ari M.
author_facet Nagy, Nina Elisabeth
Norli, Hans Ragnar
Fongen, Monica
Østby, Runa Berg
Heldal, Inger M.
Davik, Jahn
Hietala, Ari M.
author_sort Nagy, Nina Elisabeth
collection PubMed
description MAIN CONCLUSION: Lignan impregnation of the reaction zone wood protects against oxidative degradation by fungi. Traumatic resin canals may play roles in the underlying signal transduction, synthesis, and translocation of defense compounds. ABSTRACT: Tree defense against xylem pathogens involves both constitutive and induced phenylpropanoids and terpenoids. The induced defenses include compartmentalization of compromised wood with a reaction zone (RZ) characterized by polyphenol deposition, whereas the role of terpenoids has remained poorly understood. To further elucidate the tree–pathogen interaction, we profiled spatial patterns in lignan (low-molecular-weight polyphenols) and terpenoid content in Norway spruce (Picea abies) trees showing heartwood colonization by the pathogenic white-rot fungus Heterobasidion parviporum. There was pronounced variation in the amount and composition of lignans between different xylem tissue zones of diseased and healthy trees. Intact RZ at basal stem regions, where colonization is the oldest, showed the highest level and diversity of these compounds. The antioxidant properties of lignans obviously hinder oxidative degradation of wood: RZ with lignans removed by extraction showed significantly higher mass loss than unextracted RZ when subjected to Fenton degradation. The reduced diversity and amount of lignans in pathogen-compromised RZ and decaying heartwood in comparison to intact RZ and healthy heartwood suggest that α-conindendrin isomer is an intermediate metabolite in lignan decomposition by H. parviporum. Diterpenes and diterpene alcohols constituted above 90% of the terpenes detected in sapwood of healthy and diseased trees. A significant finding was that traumatic resin canals, predominated by monoterpenes, were commonly associated with RZ. The findings clarify the roles and fate of lignan during wood decay and raise questions about the potential roles of terpenoids in signal transduction, synthesis, and translocation of defense compounds upon wood compartmentalization against decay fungi. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00425-022-03842-1.
format Online
Article
Text
id pubmed-8831285
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Springer Berlin Heidelberg
record_format MEDLINE/PubMed
spelling pubmed-88312852022-02-23 Patterns and roles of lignan and terpenoid accumulation in the reaction zone compartmentalizing pathogen-infected heartwood of Norway spruce Nagy, Nina Elisabeth Norli, Hans Ragnar Fongen, Monica Østby, Runa Berg Heldal, Inger M. Davik, Jahn Hietala, Ari M. Planta Original Article MAIN CONCLUSION: Lignan impregnation of the reaction zone wood protects against oxidative degradation by fungi. Traumatic resin canals may play roles in the underlying signal transduction, synthesis, and translocation of defense compounds. ABSTRACT: Tree defense against xylem pathogens involves both constitutive and induced phenylpropanoids and terpenoids. The induced defenses include compartmentalization of compromised wood with a reaction zone (RZ) characterized by polyphenol deposition, whereas the role of terpenoids has remained poorly understood. To further elucidate the tree–pathogen interaction, we profiled spatial patterns in lignan (low-molecular-weight polyphenols) and terpenoid content in Norway spruce (Picea abies) trees showing heartwood colonization by the pathogenic white-rot fungus Heterobasidion parviporum. There was pronounced variation in the amount and composition of lignans between different xylem tissue zones of diseased and healthy trees. Intact RZ at basal stem regions, where colonization is the oldest, showed the highest level and diversity of these compounds. The antioxidant properties of lignans obviously hinder oxidative degradation of wood: RZ with lignans removed by extraction showed significantly higher mass loss than unextracted RZ when subjected to Fenton degradation. The reduced diversity and amount of lignans in pathogen-compromised RZ and decaying heartwood in comparison to intact RZ and healthy heartwood suggest that α-conindendrin isomer is an intermediate metabolite in lignan decomposition by H. parviporum. Diterpenes and diterpene alcohols constituted above 90% of the terpenes detected in sapwood of healthy and diseased trees. A significant finding was that traumatic resin canals, predominated by monoterpenes, were commonly associated with RZ. The findings clarify the roles and fate of lignan during wood decay and raise questions about the potential roles of terpenoids in signal transduction, synthesis, and translocation of defense compounds upon wood compartmentalization against decay fungi. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00425-022-03842-1. Springer Berlin Heidelberg 2022-02-10 2022 /pmc/articles/PMC8831285/ /pubmed/35142905 http://dx.doi.org/10.1007/s00425-022-03842-1 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Original Article
Nagy, Nina Elisabeth
Norli, Hans Ragnar
Fongen, Monica
Østby, Runa Berg
Heldal, Inger M.
Davik, Jahn
Hietala, Ari M.
Patterns and roles of lignan and terpenoid accumulation in the reaction zone compartmentalizing pathogen-infected heartwood of Norway spruce
title Patterns and roles of lignan and terpenoid accumulation in the reaction zone compartmentalizing pathogen-infected heartwood of Norway spruce
title_full Patterns and roles of lignan and terpenoid accumulation in the reaction zone compartmentalizing pathogen-infected heartwood of Norway spruce
title_fullStr Patterns and roles of lignan and terpenoid accumulation in the reaction zone compartmentalizing pathogen-infected heartwood of Norway spruce
title_full_unstemmed Patterns and roles of lignan and terpenoid accumulation in the reaction zone compartmentalizing pathogen-infected heartwood of Norway spruce
title_short Patterns and roles of lignan and terpenoid accumulation in the reaction zone compartmentalizing pathogen-infected heartwood of Norway spruce
title_sort patterns and roles of lignan and terpenoid accumulation in the reaction zone compartmentalizing pathogen-infected heartwood of norway spruce
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8831285/
https://www.ncbi.nlm.nih.gov/pubmed/35142905
http://dx.doi.org/10.1007/s00425-022-03842-1
work_keys_str_mv AT nagyninaelisabeth patternsandrolesoflignanandterpenoidaccumulationinthereactionzonecompartmentalizingpathogeninfectedheartwoodofnorwayspruce
AT norlihansragnar patternsandrolesoflignanandterpenoidaccumulationinthereactionzonecompartmentalizingpathogeninfectedheartwoodofnorwayspruce
AT fongenmonica patternsandrolesoflignanandterpenoidaccumulationinthereactionzonecompartmentalizingpathogeninfectedheartwoodofnorwayspruce
AT østbyrunaberg patternsandrolesoflignanandterpenoidaccumulationinthereactionzonecompartmentalizingpathogeninfectedheartwoodofnorwayspruce
AT heldalingerm patternsandrolesoflignanandterpenoidaccumulationinthereactionzonecompartmentalizingpathogeninfectedheartwoodofnorwayspruce
AT davikjahn patternsandrolesoflignanandterpenoidaccumulationinthereactionzonecompartmentalizingpathogeninfectedheartwoodofnorwayspruce
AT hietalaarim patternsandrolesoflignanandterpenoidaccumulationinthereactionzonecompartmentalizingpathogeninfectedheartwoodofnorwayspruce