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

Zhang, Jiwei; Presley, Gerald N.; Hammel, Kenneth E.; Ryu, Jae-San; Menke, Jon R.; Figueroa, Melania; Hu, Dehong; Orr, Galya; Schilling, Jonathan S.

doi:10.1073/pnas.1608454113

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

Journal Article · Mon Sep 12 00:00:00 EDT 2016 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1608454113· OSTI ID:1324321

Zhang, Jiwei; Presley, Gerald N.;

; Ryu, Jae-San; Menke, Jon R.; Figueroa, Melania;

; Orr, Galya; Schilling, Jonathan S.

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.

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Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)

Sponsoring Organization:: USDOE

Grant/Contract Number:: Early Career Grant SC0004012; BER SC0012742; User Facility grant #48607 at PNNL; AC05-76RL01830

OSTI ID:: 1324321

Alternate ID(s):: OSTI ID: 1340881

Report Number(s):: PNNL-SA-114266

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Vol. 113 Journal Issue: 39; ISSN 0027-8424

Publisher:: National Academy of Sciences, Washington, DC (United States)Copyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 124 works

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

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