Gene Regulation Shifts Shed Light on Fungal Adaption in Plant Biomass Decomposers
Abstract
ABSTRACT Fungi dominate the recycling of carbon sequestered in woody biomass. This process of organic turnover was first evolved among “white rot” fungi that degrade lignin to access carbohydrates and later evolved multiple times toward more efficient strategies to selectively target carbohydrates—“brown rot.” The brown rot adaption was often explained by mechanisms to deploy reactive oxygen species (ROS) to oxidatively attack wood structures. However, its genetic basis remains unclear, especially in the context of gene contractions of conventional carbohydrate-active enzymes (CAZYs) relative to white rot ancestors. Here, we hypothesized that these apparent gains in brown rot efficiency despite gene losses were due, in part, to upregulation of the retained genes. We applied comparative transcriptomics to multiple species of both rot types grown across a wood wafer to create a gradient of progressive decay and to enable tracking temporal gene expression. Dozens of “decay-stage-dependent” ortho-genes were isolated, narrowing a pool of candidate genes with time-dependent regulation unique to brown rot fungi. A broad comparison of the expression timing of CAZY families indicated a temporal regulatory shift of lignocellulose-oxidizing genes toward early stages in brown rot compared to white rot, enabling the segregation of oxidative treatment ahead of hydrolysis. These key brownmore »
- Authors:
- Publication Date:
- Research Org.:
- Univ. of Minnesota, Minneapolis, MN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
- OSTI Identifier:
- 1574520
- Alternate Identifier(s):
- OSTI ID: 1596520
- Grant/Contract Number:
- SC0019427; SC0012742
- Resource Type:
- Published Article
- Journal Name:
- mBio (Online)
- Additional Journal Information:
- Journal Name: mBio (Online) Journal Volume: 10 Journal Issue: 6; Journal ID: ISSN 2150-7511
- Publisher:
- American Society for Microbiology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; brown rot adaption; comparative transcriptomics; gene regulation shift; plant biomas; wood-decomposing fungi
Citation Formats
Zhang, Jiwei, Silverstein, Kevin A. T., Castaño, Jesus David, Figueroa, Melania, Schilling, Jonathan S., and Gillian Turgeon, ed., B. Gene Regulation Shifts Shed Light on Fungal Adaption in Plant Biomass Decomposers. United States: N. p., 2019.
Web. doi:10.1128/mBio.02176-19.
Zhang, Jiwei, Silverstein, Kevin A. T., Castaño, Jesus David, Figueroa, Melania, Schilling, Jonathan S., & Gillian Turgeon, ed., B. Gene Regulation Shifts Shed Light on Fungal Adaption in Plant Biomass Decomposers. United States. https://doi.org/10.1128/mBio.02176-19
Zhang, Jiwei, Silverstein, Kevin A. T., Castaño, Jesus David, Figueroa, Melania, Schilling, Jonathan S., and Gillian Turgeon, ed., B. Tue .
"Gene Regulation Shifts Shed Light on Fungal Adaption in Plant Biomass Decomposers". United States. https://doi.org/10.1128/mBio.02176-19.
@article{osti_1574520,
title = {Gene Regulation Shifts Shed Light on Fungal Adaption in Plant Biomass Decomposers},
author = {Zhang, Jiwei and Silverstein, Kevin A. T. and Castaño, Jesus David and Figueroa, Melania and Schilling, Jonathan S. and Gillian Turgeon, ed., B.},
abstractNote = {ABSTRACT Fungi dominate the recycling of carbon sequestered in woody biomass. This process of organic turnover was first evolved among “white rot” fungi that degrade lignin to access carbohydrates and later evolved multiple times toward more efficient strategies to selectively target carbohydrates—“brown rot.” The brown rot adaption was often explained by mechanisms to deploy reactive oxygen species (ROS) to oxidatively attack wood structures. However, its genetic basis remains unclear, especially in the context of gene contractions of conventional carbohydrate-active enzymes (CAZYs) relative to white rot ancestors. Here, we hypothesized that these apparent gains in brown rot efficiency despite gene losses were due, in part, to upregulation of the retained genes. We applied comparative transcriptomics to multiple species of both rot types grown across a wood wafer to create a gradient of progressive decay and to enable tracking temporal gene expression. Dozens of “decay-stage-dependent” ortho-genes were isolated, narrowing a pool of candidate genes with time-dependent regulation unique to brown rot fungi. A broad comparison of the expression timing of CAZY families indicated a temporal regulatory shift of lignocellulose-oxidizing genes toward early stages in brown rot compared to white rot, enabling the segregation of oxidative treatment ahead of hydrolysis. These key brown rot ROS-generating genes with iron ion binding functions were isolated. Moreover, transcription energy was shifted to be invested on the retained GHs in brown rot fungi to strengthen carbohydrate conversion. Collectively, these results support the hypothesis that gene regulation shifts played a pivotal role in brown rot adaptation. IMPORTANCE Fungi dominate the turnover of wood, Earth’s largest pool of aboveground terrestrial carbon. Fungi first evolved this capacity by degrading lignin to access and hydrolyze embedded carbohydrates (white rot). Multiple lineages, however, adapted faster reactive oxygen species (ROS) pretreatments to loosen lignocellulose and selectively extract sugars (brown rot). This brown rot “shortcut” often coincided with losses (>60%) of conventional lignocellulolytic genes, implying that ROS adaptations supplanted conventional pathways. We used comparative transcriptomics to further pursue brown rot adaptations, which illuminated the clear temporal expression shift of ROS genes, as well as the shift toward synthesizing more GHs in brown rot relative to white rot. These imply that gene regulatory shifts, not simply ROS innovations, were key to brown rot fungal evolution. These results not only reveal an important biological shift among these unique fungi, but they may also illuminate a trait that restricts brown rot fungi to certain ecological niches.},
doi = {10.1128/mBio.02176-19},
journal = {mBio (Online)},
number = 6,
volume = 10,
place = {United States},
year = {Tue Nov 19 00:00:00 EST 2019},
month = {Tue Nov 19 00:00:00 EST 2019}
}
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https://doi.org/10.1128/mBio.02176-19
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