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Title: Localizing gene regulation reveals a staggered wood decay mechanism for the brown rot fungus Postia placenta

Abstract

The fungi that cause brown rot of wood are essential contributors to biomass recycling in forest ecosystems. Their highly efficient cellulolytic systems, which may have practical applications, apparently depend on a combination of two mechanisms: nonselective oxidation of the lignocellulose by reactive oxygen species (ROS) coupled with hydrolysis of the polysaccharide components by a limited set of glycoside hydrolases (GHs). Since the production of strongly oxidizing ROS appears incompatible with the operation of GHs, it has been proposed that the fungi regulate ROS production by maintaining concentration gradients of the chelated metal ions they use to generate extracellular oxidants. However, calculations have indicated that this protective mechanism is physically infeasible. We examined a different hypothesis, that expression of ROS and GH components is temporally staggered by brown rot fungi in wood. We sectioned thin wafers of spruce and aspen that had been colonized directionally by Postia placenta and measured expression of relevant genes and some of the encoded enzymes, thus using the spatial distribution of fungal hyphae to resolve a fine-scale temporal sequence. Hierarchical clustering of gene expression for eight oxidoreductases thought to have a role in ROS production and of eight GHs revealed a zone of oxidoreductase upregulation atmore » the hyphal front that persisted about 48 h before upregulation of the GHs. Additional evidence for differential expression was provided by localization of endoglucanase, xylanase, mannanase, and laccase activities in the colonized wood. Our results support a two-step mechanism for brown rot, in which substrate oxidation precedes enzymatic hydrolysis.« less

Authors:
 [1];  [1]; ORCiD logo [2];  [3];  [1];  [1]; ORCiD logo [4];  [4];  [1]
  1. Univ. of Minnesota, Saint Paul, MN (United States)
  2. US Forest Products Lab., Madison, WI (United States); Univ. of Wisconsin, Madison, WI (United States)
  3. Gyeongsangnam-do Agricultural Research and Extension Services, Jinju (Republic of Korea)
  4. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
Sponsoring Org.:
USDOE
OSTI Identifier:
1324321
Alternate Identifier(s):
OSTI ID: 1340881
Report Number(s):
PNNL-SA-114266
Journal ID: ISSN 0027-8424; 49027; 48929; KP1704020
Grant/Contract Number:  
AC05-76RL01830; Early Career Grant SC0004012; BER SC0012742; User Facility grant #48607 at PNNL
Resource Type:
Journal Article: Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 113; Journal Issue: 39; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; Gene; wood decay; brown rot fungus; Postia placenta; biomass; Environmental Molecular Sciences Laboratory; biodegradation; bioconversion; decomposition; lignocellulose; cellulase

Citation Formats

Zhang, Jiwei, Presley, Gerald N., Hammel, Kenneth E., Ryu, Jae -San, Menke, Jon R., Figueroa, Melania, Hu, Dehong, Orr, Galya, and Schilling, Jonathan S.. Localizing gene regulation reveals a staggered wood decay mechanism for the brown rot fungus Postia placenta. United States: N. p., 2016. Web. doi:10.1073/pnas.1608454113.
Zhang, Jiwei, Presley, Gerald N., Hammel, Kenneth E., Ryu, Jae -San, Menke, Jon R., Figueroa, Melania, Hu, Dehong, Orr, Galya, & Schilling, Jonathan S.. Localizing gene regulation reveals a staggered wood decay mechanism for the brown rot fungus Postia placenta. United States. doi:10.1073/pnas.1608454113.
Zhang, Jiwei, Presley, Gerald N., Hammel, Kenneth E., Ryu, Jae -San, Menke, Jon R., Figueroa, Melania, Hu, Dehong, Orr, Galya, and Schilling, Jonathan S.. Mon . "Localizing gene regulation reveals a staggered wood decay mechanism for the brown rot fungus Postia placenta". United States. doi:10.1073/pnas.1608454113.
@article{osti_1324321,
title = {Localizing gene regulation reveals a staggered wood decay mechanism for the brown rot fungus Postia placenta},
author = {Zhang, Jiwei and Presley, Gerald N. and Hammel, Kenneth E. and Ryu, Jae -San and Menke, Jon R. and Figueroa, Melania and Hu, Dehong and Orr, Galya and Schilling, Jonathan S.},
abstractNote = {The fungi that cause brown rot of wood are essential contributors to biomass recycling in forest ecosystems. Their highly efficient cellulolytic systems, which may have practical applications, apparently depend on a combination of two mechanisms: nonselective oxidation of the lignocellulose by reactive oxygen species (ROS) coupled with hydrolysis of the polysaccharide components by a limited set of glycoside hydrolases (GHs). Since the production of strongly oxidizing ROS appears incompatible with the operation of GHs, it has been proposed that the fungi regulate ROS production by maintaining concentration gradients of the chelated metal ions they use to generate extracellular oxidants. However, calculations have indicated that this protective mechanism is physically infeasible. We examined a different hypothesis, that expression of ROS and GH components is temporally staggered by brown rot fungi in wood. We sectioned thin wafers of spruce and aspen that had been colonized directionally by Postia placenta and measured expression of relevant genes and some of the encoded enzymes, thus using the spatial distribution of fungal hyphae to resolve a fine-scale temporal sequence. Hierarchical clustering of gene expression for eight oxidoreductases thought to have a role in ROS production and of eight GHs revealed a zone of oxidoreductase upregulation at the hyphal front that persisted about 48 h before upregulation of the GHs. Additional evidence for differential expression was provided by localization of endoglucanase, xylanase, mannanase, and laccase activities in the colonized wood. Our results support a two-step mechanism for brown rot, in which substrate oxidation precedes enzymatic hydrolysis.},
doi = {10.1073/pnas.1608454113},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 39,
volume = 113,
place = {United States},
year = {Mon Sep 12 00:00:00 EDT 2016},
month = {Mon Sep 12 00:00:00 EDT 2016}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at 10.1073/pnas.1608454113

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Cited by: 11 works
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Works referenced in this record:

Comparative genomics of Ceriporiopsis subvermispora and Phanerochaete chrysosporium provide insight into selective ligninolysis
journal, March 2012

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